Plant Life under Changing Environment: Responses and Management [1 ed.] 0128182040, 9780128182048

Table of contents :
Cover
Plant Life Under Changing Environment: Responses and Management
Copyright
Contents
List of contributors
1 Abiotic stress–induced programmed cell death in plants
1.1 Introduction
1.2 Relation between reactive oxygen species and programmed cell death
1.3 Programmed cell death–related proteases
1.4 Abiotic stress and programmed cell death
1.4.1 High and low temperature–induced programmed cell death
1.4.2 Drought- and flooding-induced programmed cell death
1.4.3 Salinity-induced programmed cell death
1.4.4 Ultraviolet-induced programmed cell death
1.4.5 Heavy metal- and nanoparticle-induced programmed cell death
1.5 Concluding remarks and future perspectives
References
2 Regulation of temperature stress in plants
2.1 Introduction
2.2 Effect of temperature stress on plants
2.2.1 High temperature
2.2.2 Low temperature
2.3 Plant adaptations to heat stress
2.3.1 Physiological adaptation
2.3.2 Biochemical adaptation
2.3.3 Molecular adaptation
2.3.4 Nutrient management approach
2.3.4.1 Role of macronutrients
2.3.4.2 Role of micronutrients
2.4 Conclusion
References
Further reading
3 Salinity and its tolerance strategies in plants
3.1 Introduction
3.1.1 Plants and salt stress
3.2 Genesis and classification of saline soils
3.2.1 Genesis of saline soil
3.2.2 Sources of saline soils
3.2.3 Classification of saline soils
3.3 Effects of salinity and sodicity on soil physicochemical attributes
3.3.1 Effect on sodicity on soil physical and chemical properties
3.3.2 Effect on salinity on soil physical and chemical properties
3.4 Effect of salinity on plant growth
3.4.1 Osmotic deregulations
3.4.2 Specific ion toxicity
3.5 Plant responses to salinity
3.5.1 Physiological adaptation
3.5.1.1 Stomatal conductance and photosynthetic activity
3.5.2 Biochemical adaptation
3.5.2.1 Osmotic regulations
3.5.2.2 Oxidative modification
3.5.2.3 Intercellular signaling
3.5.2.4 Hormone regulation
3.5.2.4.1 Hormonal-modified proline metabolism and plant growth
3.5.2.4.1.1 Abscisic acid
3.5.2.4.1.2 Ethylene
3.5.2.4.1.3 Salicylic acid
3.5.2.4.1.4 Nitric oxide
3.5.3 Cellular mechanisms
3.5.3.1 Na+ exclusion from the cell
3.5.3.2 Na+ transporters
3.5.4 Tissue tolerance to ions
3.5.4.1 Solute accumulation in cells
3.5.4.1.1 Compartmentation of Na+ inside cell
3.5.4.1.2 Homeostasis
3.5.4.1.3 Apoplastic alkalization and reacidulation
3.6 Microbe–plant interaction
3.6.1 Plant growth-promoting rhizobacteria
3.6.1.1 Hormone production for enhanced growth
3.6.2 Halotolerant microbe–mediated processes
3.6.3 Fungal–plant interaction
3.6.3.1 Arbuscular mycorrhizae in salt-affected soils
3.6.3.2 Impact of arbuscular mycorrhizae–plant association on plant growth
3.7 Effect of different amendments in tolerance against salinity
3.7.1 Organic amendments
3.7.2 Inorganic amendments
3.8 Genetic modification in plants to enhance tolerance against salinity
3.9 Genetic engineering of halotolerant plants
3.10 Summary
References
Further reading
4 Regulation of drought stress in plants
4.1 Introduction
4.2 Causes of drought
4.3 Impacts of drought
4.3.1 Impact on global agriculture
4.3.1.1 Impacts on individual plant
4.3.1.1.1 Metabolic changes
4.3.1.1.2 Physiological changes
4.4 Combating with drought
4.4.1 Soil features
4.4.1.1 Soil biota activity
4.4.1.2 Soil physicochemical activities
4.4.1.3 Plant mechanism to cope with drought
4.4.1.3.1 Signaling of stress
4.4.1.3.2 Growth and physiological modification
4.4.1.3.3 Dehydration avoidance and tolerance
4.4.1.3.4 Nutrient acquisition habits
4.4.1.3.5 Biochemical responses
4.4.1.3.6 Protein synthesis such as heat-shock proteins
4.4.1.3.7 Antioxidant response
4.4.1.3.8 Metabolic responses
4.4.1.3.9 Cellular responses
4.4.1.3.10 Gene induction and expression
4.4.1.3.11 Organelle response
4.4.2 Exogenous amendments for combating drought
4.4.2.1 Organic amendments
4.4.2.2 Inorganic amendments
4.4.3 Microbe plant interactions
4.4.3.1 Plant growth–promoting rhizobacteria
4.4.3.1.1 Phytohormone production
4.4.3.1.2 Root growth modification
4.4.3.1.3 Osmolytes accumulation in plant tissue
4.4.3.1.4 Drought tolerance gene induction in plants
4.4.3.2 Mycorrhizal association
4.4.4 Genetic engineering of drought-tolerant crops
4.5 Salient features of drought-tolerant plants
4.6 Summary
References
5 Plant responses to radiation stress and its adaptive mechanisms
5.1 Introduction
5.2 Plants and their environment
5.2.1 Source of life on earth
5.2.2 Types and sources of radiation
5.2.2.1 Alpha radiation
5.2.2.2 Beta radiation
5.2.2.3 Gamma radiation
5.2.2.4 X-rays
5.2.2.5 Ultraviolet radiation
5.3 Effect of radiations
5.3.1 Morphological and physiological effects
5.3.2 Biochemical changes
5.3.3 Molecular damages
5.4 Mitigating strategies
5.4.1 Endogenous strategies
5.4.2 Ultraviolet shielding and behavioral escape mechanisms
5.4.3 Ultraviolet-B as a protectant in plants
5.4.4 Transduction of signal via ultraviolet damage
5.4.5 Plant hormones as protectants against harmful radiation
5.5 Conclusion
References
Further reading
6 Regulation of low phosphate stress in plants
6.1 Introduction
6.2 Morphological responses under low inorganic phosphate stress
6.2.1 Changes in root system architecture
6.2.2 Mechanism of root system architecture modification under low inorganic phosphate stress condition
6.2.2.1 Mechanism of changes in primary root growth
6.2.2.2 Mechanism of changes in lateral root growth
6.2.2.3 Mechanism of changes in root hairs
6.3 Molecular responses to low phosphate stress
6.3.1 Induction of phosphate transporter genes by low inorganic phosphate stress
6.3.1.1 Phosphate Transporter1
6.3.1.1.1 Structural insights of Phosphate Transporter1 transporters
6.3.1.2 Phosphate Transporter2
6.3.1.3 Phosphate Transporter3
6.3.1.4 Phosphate Transporter4
6.3.1.5 Phosphate Transporter5; vacuolar inorganic phosphate transporter1
6.3.2 PHOSPHATE1; the inorganic phosphate exporter
6.3.3 Transcription factors
6.3.4 MicroRNAs
6.4 Role of arbuscular mycorrhizae fungal in low phosphate stress tolerance
6.5 Biochemical responses to low phosphate stress
6.5.1 Hormones
6.5.2 Sugars
6.5.3 Inositol pyrophosphates
6.5.4 Lipids
6.5.5 Exudation of organic acids from roots
6.5.6 Release of acid phosphatases
6.6 Conclusion and future prospects
References
7 Regulation of flood stress in plants
7.1 Introduction
7.2 Plants strategies against flooding stress
7.2.1 Escape strategy under submergence
7.2.2 Quiescence strategy under submergence
7.2.3 Water logging tolerance strategy
7.3 Flooding tolerance mechanisms
7.3.1 Morphological response
7.3.2 Endogenous hormonal response
7.3.2.1 Gibberellins
7.3.2.2 Ethylene
7.3.2.3 Abscisic acid
7.3.2.4 Salicylic acid
7.3.3 Genetic response
7.4 Conclusion
References
Further reading
8 Heavy metals, water deficit, and their interaction in plants: an overview
8.1 Introduction
8.2 Heavy-metal effects on plants
8.2.1 Essential heavy-metal elements
8.2.1.1 Copper
8.2.1.2 Zinc
8.2.1.3 Iron
8.2.1.4 Manganese
8.2.1.5 Nickel
8.2.1.6 Cobalt
8.2.1.7 Molybdenum
8.2.2 Toxic heavy metals
8.2.2.1 Cadmium
8.2.2.2 Lead
8.2.2.3 Mercury
8.2.2.4 Chromium
8.3 Water-deficit stress in plants
8.3.1 Growth attributes of plants affected by water deficit
8.3.2 Photosynthetic performance under water deficit
8.3.3 Antioxidative defense mechanism under water-deficit stress
8.3.4 Role of osmotic adjustment and accumulation of solutes tolerant to dehydration
8.4 Combination of metal with water-deficit stress
8.4.1 The combined impact of metal and water deficit on plant growth and physiological processes
8.4.2 Plant–water relations under metal stress
8.5 Conclusions and future perspective
References
Further reading
9 Genetic engineering approaches and applicability for the bioremediation of metalloids
9.1 Introduction
9.2 Sources of metals
9.3 Metals: occurrence, speciation, and toxic effects
9.3.1 Lead
9.3.2 Mercury
9.3.3 Cadmium
9.3.4 Arsenic
9.3.5 Chromium
9.4 Remediation of toxic metals and metalloids
9.5 Bioremediation
9.5.1 Ex situ bioremediation
9.5.1.1 Slurry-phase bioremediation
9.5.1.2 Solid-phase bioremediation
9.5.2 In situ bioremediation
9.5.2.1 Intrinsic in situ bioremediation
9.5.2.2 Engineered in situ bioremediation
9.5.3 Bioremediation technologies
9.5.3.1 Bioventing
9.5.3.2 Biosparging
9.5.3.3 Bioaugmentation
9.5.3.4 Bioslurping
9.5.3.5 Biofilters
9.5.3.6 Biostimulation
9.5.3.7 Land farming
9.5.3.8 Composting
9.6 Phytoremediation
9.6.1 Phytodegradation
9.6.2 Phytostimulation
9.6.3 Phytostabilization
9.6.4 Phytovolatilization
9.6.5 Phytoextraction
9.6.6 Rhizofiltration
9.7 Genetic engineering and its application in the bioremediation of toxic metals
9.7.1 Mercury
9.7.2 Arsenic
9.7.3 Cadmium
9.7.4 Lead
9.8 Conclusion
References
Further reading
10 Responses of plants to herbicides: Recent advances and future prospectives
10.1 Introduction
10.2 Phenotypical manifestation
10.3 Herbicides: a multifaceted chemical
10.4 Physiological damage through generated reactive oxygen species intermediates
10.4.1 Protein oxidation
10.4.2 Lipid peroxidation
10.4.3 Antioxidant defense in response to herbicide treatment
10.5 Direct damage to the physiological process
10.5.1 Photosystem II inhibitor
10.5.2 Photosystem I inhibitors
10.5.3 Amino acid biosynthesis
10.6 Chlorophyll and carotenoid biosynthesis
10.7 Conclusions
References
11 Effects of abiotic stresses on sugarcane plants with emphasis in those produced by wounds and prolonged post–harvest periods
11.1 Introduction
11.2 Heat and cold stress
11.3 Nutrition-related stresses
11.4 Salt stress
11.5 Drought
11.6 Stress produced by mechanical injuries
11.7 Sucrose synthesis and partitioning during abiotic stress
11.8 Conclusions and future prospects
References
Further reading
12 Heavy metal stress and plant life: uptake mechanisms, toxicity, and alleviation
12.1 Introduction
12.2 Sources and metal bioavailability
12.3 Consequences of heavy metals in plants
12.4 Mechanisms of heavy metals uptake and transport in plants
12.5 Mechanism of heavy metals detoxification/tolerance in plants
12.6 Avoidance mechanisms
12.7 Metal binding to cell wall
12.8 Tolerance mechanisms
References
Further reading
13 Nanoparticles in plants: morphophysiological, biochemical, and molecular responses
13.1 Introduction
13.2 Nanotechnology and nanoparticles
13.3 Impacts of nanoparticles in plants
13.3.1 Morphological, anatomical, and histological changes induced by nanoparticles
13.3.2 Induction of antioxidant compounds by nanoparticles
13.3.2.1 Oxidative stress
13.3.2.2 Antioxidant capacity
13.3.2.3 Oxidative stress induced by nanoparticles
13.3.2.4 Induction of antioxidant capacity by nanoparticles
13.3.2.4.1 Enzyme compounds
13.3.2.4.2 Nonenzymatic compounds
13.3.2.5 Induction of tolerance to abiotic stress through increased antioxidant capacity
13.3.3 Transcriptomic and proteomic responses of plants to nanoparticles and abiotic stress
13.3.3.1 Transcriptomic modifications by nanoparticles and abiotic stress
13.3.3.2 Proteomic modifications of plants exposed to nanoparticles
13.3.4 Positive effects of nanoparticles on agronomical aspects of crops
13.4 Conclusion
References
14 Regulations of reactive oxygen species in plants abiotic stress: an integrated overview
14.1 Introduction
14.2 Reactive oxygen species regulation in plant organelles during abiotic stress
14.2.1 Chloroplasts
14.2.2 Mitochondria
14.2.3 Peroxisomes
14.2.4 Apoplasts
14.2.5 Other sources
14.3 Antioxidants involved in stress-induced regulation of reactive oxygen species
14.3.1 Enzymatic antioxidants
14.3.2 Nonenzymatic antioxidants
14.4 Signaling roles of reactive oxygen species in plants under abiotic stress
14.4.1 Reactive oxygen species signal perception
14.4.2 Transduction and Interaction of reactive oxygen species signaling
14.5 Conclusion and future prospects
References
Further reading
15 Plant–microbe interactions in plants and stress tolerance
15.1 Introduction
15.2 Salinity stress
15.2.1 Plant growth–promoting rhizobacteria and alleviation of salinity stress in plants
15.2.1.1 Production of phytohormones
15.2.1.2 Decreased salinity stress–induced ethylene production
15.2.1.3 Increase in plant nutrients uptake
15.2.1.4 Accumulation of osmolytes in plants
15.2.1.5 Ion homeostasis in plants
15.2.1.6 Induction of antioxidative enzymes
15.2.1.7 Production of exopolysaccharides (EPS)
15.2.1.8 Induction of systemic tolerance
15.3 Drought stress
15.3.1 Plant growth–promoting rhizobacteria and alleviation of drought stress
15.3.1.1 Modifications in phytohormonal content
15.3.1.2 Decreased stress-induced ethylene production
15.3.1.3 Induced plant synthesis of antioxidative enzymes
15.3.1.4 Osmolytes (compatible solutes) accumulation
15.3.1.5 Generation of exopolysaccharides (EPS)
15.4 Heavy metal toxicity stress
15.4.1 Plant growth–promoting rhizobacteria and alleviation of heavy metals toxicity stress in plants
15.4.1.1 Generation of siderophores
15.4.1.2 Synthesizing 1-aminocyclopropane-1-carboxylate deaminase
15.4.1.3 Phosphate solubilization
15.4.1.4 Production of organic acids
15.4.1.5 Biosurfactant production
15.4.1.6 Generation of phytohormones
15.4.1.7 Betterment in the uptake of micro- and macronutrients
15.4.1.8 Production of exopolymers
15.4.1.9 Diminished uptake of heavy metals
15.4.1.10 Heavy metals–resistant genes induction
15.5 Mineral nutritional imbalance stress
15.5.1 Plant growth–promoting rhizobacteria and the availability of nutrients
15.5.1.1 Nitrogen
15.5.1.2 Phosphorus
15.5.1.3 Potassium
15.5.1.4 Microelements (trace minerals)
15.6 Conclusions and future prospects
References
16 Phytohormonal signaling under abiotic stress
16.1 Introduction
16.2 Abscisic acid
16.3 Abscisic acid biosynthesis
16.4 Abscisic acid signaling
16.5 Abscisic acid–dependent signal transduction
16.6 Abscisic acid–independent signal transduction
16.7 Auxin
16.8 Auxin biosynthesis
16.9 Auxin signaling
16.10 Brassinosteroids
16.11 Brassinosteroid biosynthesis
16.12 Brassinosteroids signaling
16.13 Ethylene
16.14 Ethylene biosynthesis
16.15 Ethylene signaling
16.16 Gibberellins
16.17 Gibberellin biosynthesis
16.18 Gibberellin signaling
16.19 Cytokinin
16.20 Cytokinins biosynthesis
16.21 Cytokinin signaling
16.22 Jasmonic acid and salicylic acid
16.23 Jasmonic acid biosynthesis
16.24 Salicylic acid biosynthesis
16.25 Jasmonic acid signaling
16.26 Salicylic acid signaling
16.27 Nitric oxide
16.28 NO biosynthesis
16.29 NO signaling
16.30 Strigolactones
16.31 Strigolactone biosynthesis
16.32 Strigolactone signaling
16.33 Karrikins
16.34 Karrikin signaling
16.35 Cross talk between phytohormone signaling
References
Further reading
17 Role of sRNAs in abiotic stress tolerance
17.1 Introduction
17.2 sRNA
17.3 Biogenesis and mechanism of action of sRNAs
17.4 Mechanism of sRNA-mediated gene regulation
17.4.1 Transcriptional gene silencing
17.4.2 Posttranscriptional gene silencing
17.5 Role of mRNAs in stress tolerance
17.6 Role of small interfering RNAs in defense against pathogen
17.7 Role of sRNAs (lncRNAs—a type) in vernalization
17.8 Role of sRNAs in the development of leaf and leaf size and morphology
17.9 Role of sRNAs in alleviating salt stress
17.10 Role of sRNAs in oxidative stress regulation
17.11 Role of sRNAs in signaling of hormone
17.12 Conclusion
References
Further reading
18 Role of polyamines in plants abiotic stress tolerance: Advances and future prospects
18.1 Introduction
18.2 Synthesis of polyamines under abiotic stresses
18.3 Metabolism of polyamine during different stress conditions
18.4 Polyamines and abiotic stress tolerance in plants
18.5 Polyamine accumulating transgenic plants with improved abiotic stress tolerance
18.6 Polyamines role in response to different abiotic stresses
18.6.1 Metal stress
18.6.2 Osmotic, salinity, heat, and/or cold stress
18.7 Polyamine treatment modulated plant-stress tolerance
18.8 Conclusion and future perspectives
References
19 The role of sugars in the regulation of environmental stress
19.1 Introduction
19.1.1 Plant growth and development
19.1.2 Role of sugars in processes of plants physiology
19.1.2.1 Photosynthesis
19.1.2.2 Senescence
19.1.2.3 Seed germination
19.1.2.4 Flowering
19.1.2.5 Hypocotyl growth
19.1.3 Sugar sensing and signaling
19.1.4 Signal-transduction cascades
19.1.5 Sugars and abiotic stress interaction in plants
19.1.5.1 Effects of water deficit
19.1.5.2 Effects of salinity (NaCl)
19.1.5.3 Effects of light
19.1.5.4 Effects of low temperatures
19.1.5.5 Oxidative stress and antioxidant system
19.1.6 Conclusions and future perspectives
References
20 Proteomics in relation to abiotic stress tolerance in plants
20.1 Introduction
20.2 Understanding and identifying key metabolic proteins associated with abiotic stresses
20.2.1 Proteins and genes associated with signaling cascades and transcriptional regulation
20.2.2 Proteins and genes with roles in the protection of membranes
20.2.3 Proteins involved in water and ion uptake and transport
20.3 Effect of reactive oxygen species on protein modification
20.3.1 Posttranslational modifications
20.3.1.1 Phosphorylation
20.3.1.2 Glycosylation
20.3.1.3 Acetylation
20.3.1.4 Succinylation
20.3.2 Other posttranslational modifications of crop proteins
20.3.2.1 Histone
20.3.2.2 Tubulin
20.3.3 Reactive oxygen species–induced protein oxidative modifications
20.3.3.1 Sulfonylation
20.3.3.2 Glutathionylation
20.3.3.3 Tryptophan oxidation
20.3.3.4 Carbonylation
20.3.3.5 Nitrosylation
20.4 Regulation of protein stability
20.4.1 Hormone-mediated stress tolerance in plants
20.4.1.1 Auxin
20.4.1.2 Brassinosteroids
20.4.1.3 Gibberellins
20.4.1.4 Abscisic acid
20.4.2 Ubiquitin protease system
20.4.3 Calmodulin-mediated alterations
20.5 Overexpression of organelle proteins in transgenic plants improves stress tolerance
20.6 Synthesis of the novel proteins
20.7 Conclusion and future aspects
References
Further reading
21 Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects
21.1 Introduction
21.2 Phytohormone biosynthesis and signaling pathways
21.2.1 Auxin
21.2.2 Abscisic acid
21.2.3 Brassinosteroids
21.2.4 Cytokinin
21.2.5 Gibberellic acid
21.2.6 Ethylene
21.2.7 Jasmonic acid
21.2.8 Salicylic acid
21.3 Regulatory mechanism of phytohormones
21.4 Phytohormone-mediated modulation in plant under certain abiotic stresses
21.4.1 Heavy metal stress
21.4.2 Water stress
21.4.3 Salt stress
21.4.4 Ultraviolet-B stress
21.5 Future perspective
References
22 Abiotic-stress tolerance in plants-system biology approach
22.1 Introduction
22.2 Abiotic stresses and their impact on plant growth and metabolism
22.3 Systems biology approaches for improvement of plant’s abiotic-stress tolerance
22.3.1 Genomics
22.3.2 Transcriptomics
22.3.3 Proteomics
22.3.4 Metabolomics
22.3.5 Interactomics
22.3.6 Other “omics” approaches
22.4 Integration of multiple “omics” data
22.4.1 Transcriptomic–proteomic
22.4.2 Transcriptomic–metabolomic
22.4.3 Metabolomic–proteomic
22.5 Modeling and simulation in plant system dynamics
22.5.1 Gene-to-metabolite networks
22.5.2 Protein–protein interaction networks
22.5.3 Transcriptional regulatory networks
22.5.4 Gene regulatory networks
22.5.5 Coexpression networks
22.6 Software and algorithms for plant systems biology
22.6.1 Data handling and analysis
22.6.2 Visualization of plant omics data
22.6.3 Storage and maintenance of data and results
22.7 Conclusion and future prospects
References
Further reading
23 Plant single-cell biology and abiotic stress tolerance
23.1 Introduction
23.1.1 Need of plant single-cell biology approach
23.2 Single-cell models
23.2.1 Male and female gametophytes
23.2.2 Guard cells
23.2.3 Trichomes
23.3 Computational biology to study plant single-cell responses and abiotic stress tolerance
23.4 Techniques to study single-cell response to abiotic stress
23.4.1 Microelectrode ion flux estimation technique
23.4.1.1 Usage of microelectrode ion flux estimation to study cell response under abiotic stresses
23.4.1.1.1 Salt stress
23.4.1.1.2 Water deficit and oxygen deprivation
23.4.1.1.3 Aluminum stress
23.4.2 Single-cell genomic analysis
23.5 Concluding remarks
References
Further reading
24 Nanoparticle application and abiotic-stress tolerance in plants
24.1 Introduction
24.2 Uptake, transportation, and translocation of nanoparticles
24.2.1 Nanoparticle application and oxidative stress tolerance
24.3 Nanoparticle application and its role in redox regulation
24.4 Nanoparticle application and photosynthetic apparatus
24.5 Nanoparticles application and ionic homeostasis
24.6 Nanoparticles toxicity in plants
24.7 Conclusion
References
Further reading
25 The role of aquaporins during plant abiotic stress responses
25.1 Introduction
25.2 Brief history of aquaporins
25.3 Aquaporins: functional and structural significance in plants
25.4 Water dynamics and aquaporins
25.5 Roles of aquaporins in abiotic stresses
25.5.1 Aquaporins in drought/desiccation stress
25.5.2 Aquaporins in salinity stress
25.5.3 Aquaporins in low temperature stress
25.5.4 Aquaporins in trace element transport and heavy-metal toxicity
25.6 Conclusion and future perspectives
References
26 Tolerance mechanisms of medicinal plants to abiotic stresses
26.1 The concept of increased resistance to abiotic stresses in medicinal plants
26.2 Tolerance to drought stress
26.3 Tolerance to salt stress
26.4 The mechanism of resistance to light stress and UV in medicinal plants
26.5 The resistance mechanism of medicinal and aromatic plants to temperature stress
26.6 Heat stress
26.7 Cold stress
26.8 Heavy metal stress
26.9 Conclusion
References
Further reading
27 Regulation of the Calvin cycle under abiotic stresses: an overview
27.1 Introduction
27.1.1 The Calvin–Benson–Bassham cycle
27.1.1.1 Calvin cycle enzymes
27.2 Regulation of the Calvin cycle and its enzymes under abiotic stresses
27.2.1 Water stress
27.2.2 Salt stress
27.2.3 Temperature stress
27.2.3.1 High temperature
27.2.3.2 Low temperature
27.2.4 Heavy metal stress
27.2.5 Ozone stress
27.2.6 UV-B stress
27.3 Conclusion and future perspectives
References
Further reading
28 Roles of microRNAs in plant development and stress tolerance
28.1 Introduction
28.2 Biogenesis of microRNAs
28.3 Role of microRNAs in plant growth and development
28.4 Role of microRNAs in various abiotic stresses
28.5 MicroRNAs and heavy-metal stress
28.6 MicroRNAs and oxidative stress
28.7 MicroRNAs and drought stress
28.8 MicroRNAs and salt stress
28.9 MicroRNAs and UV-B radiation
28.10 MicroRNAs and temperature stress
28.11 Conclusion and future outlook
References
Further reading
29 Nitric oxide under abiotic stress conditions
29.1 Introduction
29.2 Nitric oxide sources under abiotic stress
29.2.1 Oxidative pathway
29.2.1.1 Nitric oxide–like synthase
29.2.1.2 Polyamines
29.2.2 Reductive pathway
29.2.2.1 Nonenzymatic
29.2.2.2 Nitrate reductase
29.2.2.3 Other reductive pathways
29.3 Nitric oxide signaling under abiotic stress
29.3.1 Salinity
29.3.2 Nitric oxide is a long-distance signal during wounding stress
29.3.3 Heat stress
29.3.4 Low temperatures
29.3.5 Heavy metals
29.3.6 Drought
29.3.7 Nitric oxide and ozone stress
29.4 Conclusion and perspectives
References
30 Role of metabolites in abiotic stress tolerance
30.1 Abiotic stress tolerance
30.2 Primary metabolites and osmoprotectants
30.2.1 Carbohydrates
30.2.1.1 Trehalose
30.2.1.2 Starch
30.2.1.3 Fructans
30.2.1.4 Raffinose family oligosaccharides
30.2.2 Amino acids
30.2.2.1 Proline
30.2.2.2 γ-Amino-N-butyric acid
30.2.3 Sugar alcohols (polyols): myo-inositol, d-pinitol
30.2.3.1 Cyclitols: myo-inositol and pinitol
30.2.3.2 Alditols: mannitol and sorbitol
30.2.4 Glycine betaine, an osmotic adjustment substance
30.2.5 Polyamines
30.2.6 New players in abiotic stress tolerance: melatonin and serotonin
30.2.6.1 Melatonin
30.2.6.2 Serotonin
30.3 Role of secondary metabolites: antioxidants and defense compounds
30.4 Conclusions and future prospects
References
31 Role of melatonin and serotonin in plant stress tolerance
31.1 Introduction
31.2 Tryptophan metabolism: biosynthesis of phyto-serotonin and melatonin
31.3 Fate of melatonin and serotonin in plants
31.4 Plant stress physiology and role of indolamines
31.4.1 Environmental stresses
31.4.1.1 Temperature stress
31.4.1.2 Water stress
31.4.1.3 UV stress
31.4.2 Chemical stress
31.4.2.1 Heavy metal stress
31.4.2.2 Salinity stress
31.4.3 Biological stress
31.5 Conclusion
References
32 Role of nitric oxide–dependent posttranslational modifications of proteins under abiotic stress
32.1 Introduction
32.2 Nitric oxide–dependent posttranslational modification of proteins under abiotic stress
32.2.1 Protein S-nitrosylation under adverse environmental stress conditions
32.2.1.1 Extreme temperatures
32.2.1.2 Wounding
32.2.1.3 Salinity
32.2.1.4 Heavy metals
32.2.1.5 Ozone
32.2.2 Protein tyrosine nitration during abiotic stress situations
32.2.2.1 Extreme temperatures
32.2.2.2 Wounding
32.2.2.3 Salinity
32.2.2.4 Heavy metals
32.2.3 Nitrated fatty acids
32.2.3.1 Protein nitroalkylation
32.3 Conclusions and perspectives
References
Further reading
33 Regulatory role of circadian clocks in plant responses to abiotic stress
33.1 Introduction
33.2 Role of the circadian clock in regulating plant stress responses
33.2.1 Circadian clock regulates plant response to salt stress
33.2.2 Circadian clock regulates plant response to drought stress
33.2.3 Circadian clock regulates plant response to cold stress
33.3 Circadian clock regulates stress-responsive genes
33.4 Abiotic stress affects clock genes transcription
33.5 Circadian clock mediates hormone signaling
References
Further reading
34 Regulation of genes and transcriptional factors involved in plant responses to abiotic stress
34.1 Introduction
34.2 Gene regulation and transcriptional factors in plant response to salt stress
34.3 Regulation of genes and transcriptional factors in plant response to drought stress
34.4 Heavy metal stress and its transcriptional factors regulation
34.5 Genes and transcriptional factors regulation of chilling and cold stress
34.6 Gene regulation of waterlogging tolerance
34.7 Transcriptional factors regulation of flooding stress
References
Further reading
35 Role of ionomics in plant abiotic stress tolerance
35.1 Introduction
35.2 Forward genetics and ionomic gene identification
35.2.1 Natural resources and ionomic alleles identification
35.3 Effect of heavy metal on plants
35.3.1 Mechanism of heavy metal toxicity in plants
35.4 Toxicity of heavy metals in plants
35.5 Ionomics of heavy metals
35.5.1 P1B-ATPases/heavy metal ATPases
35.5.2 Natural resistance-associated macrophage protein transporters
35.5.3 Cation diffusion facilitators/Metal tolerance proteins
35.5.4 ZRT, IRT-like proteins transporters
35.6 Salt stress and plants
35.7 Role of osmolytes in plant protection
35.7.1 Role of late-embryogenesis-abundant- type proteins in salt stress
35.8 Ionomics of salt stress
35.8.1 HKT-type Na+ transporters
35.8.2 V-type H+ ATPases
35.9 Effect of osmotic stress on plants
35.10 Ionomics of osmotic stress
References
Further reading
36 Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture
36.1 Introduction
36.1.1 Growth attributes by plant growth-promoting rhizobacteria
36.1.2 Mode of action for PGPR
36.2 Direct mechanism
36.2.1 N2 fixation
36.2.2 Phosphate solubilization
36.2.3 Siderophore production
36.2.4 Phytohormone production
36.2.5 ACC deaminase production
36.3 Indirect mechanism
36.3.1 Root exudation strengthens synergy with rhizobacteria
36.3.2 Impact of nanoparticles stress over rhizobacteria
36.3.3 Rhizospheric bacteria in abiotic stress
Conclusion
References
Further reading
37 Management of abiotic stress and sustainability
37.1 Introduction
37.2 Economic effects of the most disturbed abiotic stress
37.3 Drought
37.4 Temperature
37.5 Flooding
37.6 Salinity
37.7 Greenhouse gas
37.8 Management of abiotic stress
37.9 Breeding
37.10 Fertilizers
37.11 Management of impacts of abiotic stress in southeast Mediterranean Sea
37.12 Mathematical model of future of sugar beet industry (FOSI) in North Egypt
37.13 Optimal solutions
References
Further reading
Appendix
38 Use of quantitative trait loci to develop stress tolerance in plants
38.1 Introduction
38.2 Types of abiotic stress in plants
38.2.1 Drought stress
38.2.1.1 Hormonal response under drought
38.2.1.2 Water-use and photosynthetic activity under drought
38.2.1.3 Osmotic adjustment under drought
38.2.1.4 Root responses under drought
38.2.1.5 Yield responses under drought
38.2.2 Mineral stress
38.2.2.1 Quantitative trait loci related to macro-minerals
38.2.2.1.1 Nitrogen deficiency quantitative trait loci
38.2.2.1.2 Phosphorus deficiency quantitative trait loci
38.2.2.1.3 Potassium deficiency quantitative trait loci
38.2.2.2 Quantitative trait loci related to micro-nutrients
38.2.2.2.1 Iron (Fe) deficiency quantitative trait loci
38.2.2.2.2 Manganese deficiency quantitative trait loci
38.2.2.2.3 Boron deficiency quantitative trait loci
38.2.2.2.4 Zinc deficiency quantitative trait loci
38.2.3 Mineral toxicity
38.2.3.1 Aluminum
38.2.3.2 Cadmium
38.2.3.3 Selenium
38.2.3.4 Boron
38.2.3.5 Iron
38.2.3.6 Chromium
38.2.3.7 Manganese
38.2.3.8 Zinc
38.2.3.9 Copper
38.2.4 Heat stress
38.2.5 Cold stress
38.2.6 Salinity stress
38.2.7 Flooding/waterlogging/submergence tolerance
38.2.8 Stay-green attribute
38.3 Concluding remarks and future perspectives
References
Further reading
Index
Back Cover

Citation preview

PLANT LIFE UNDER CHANGING ENVIRONMENT

PLANT LIFE UNDER CHANGING ENVIRONMENT Responses and Management Edited by

DURGESH KUMAR TRIPATHI Amity Institute of Organic Agriculture, Amity University Uttar Pradesh, Noida, India

VIJAY PRATAP SINGH Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, India

DEVENDRA KUMAR CHAUHAN D D Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Prayagraj, India

SHIVESH SHARMA Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India

SHEO MOHAN PRASAD Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India

NAWAL KISHORE DUBEY Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, India

NALEENI RAMAWAT Amity Institute of Organic Agriculture, Amity University Uttar Pradesh, Noida, India

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright © 2020 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN: 978-0-12-818204-8 For Information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Charlotte Cockle Acquisitions Editor: Nancy Maragioglio Editorial Project Manager: Kelsey Connors Production Project Manager: Punithavathy Govindaradjane Cover Designer: Miles Hitchen Typeset by MPS Limited, Chennai, India

Contents 3.7 Effect of different amendments in tolerance against salinity 62 3.8 Genetic modification in plants to enhance tolerance against salinity 63 3.9 Genetic engineering of halotolerant plants 63 3.10 Summary 64 References 64 Further reading 75

List of contributors xiii 1. Abiotic stress induced programmed cell death in plants Fatma Yanık, Aslıhan C ¸ etinba¸s-Genc¸ and Filiz Vardar

1.1 Introduction 1 1.2 Relation between reactive oxygen species and programmed cell death 3 1.3 Programmed cell death related proteases 6 1.4 Abiotic stress and programmed cell death 8 1.5 Concluding remarks and future perspectives 16 References 16

4. Regulation of drought stress in plants Zia Ur Rahman Farooqi, Muhammad Ashar Ayub, Muhammad Zia ur Rehman, Muhammad Irfan Sohail, Muhammad Usman, Hinnan Khalid and Komal Naz

4.1 Introduction 77 4.2 Causes of drought 78 4.3 Impacts of drought 79 4.4 Combating with drought 84 4.5 Salient features of drought-tolerant plants 94 4.6 Summary 94 References 95

2. Regulation of temperature stress in plants Sanjesh Tiwari, Anuradha Patel, Madhulika Singh and Sheo Mohan Prasad

2.1 Introduction 25 2.2 Effect of temperature stress on plants 2.3 Plant adaptations to heat stress 33 2.4 Conclusion 40 References 40 Further reading 45

27

5. Plant responses to radiation stress and its adaptive mechanisms Shikha Singh, Abreeq Fatima, Santwana Tiwari and Sheo Mohan Prasad

5.1 Introduction 105 5.2 Plants and their environment 5.3 Effect of radiations 109 5.4 Mitigating strategies 113 5.5 Conclusion 119 References 119 Further reading 122

3. Salinity and its tolerance strategies in plants Muhammad Ashar Ayub, Hamaad Raza Ahmad, Mujahid Ali, Muhammad Rizwan, Shafaqat Ali, Muhammad Zia ur Rehman and Aisha A. Waris

3.1 Introduction 47 3.2 Genesis and classification of saline soils 48 3.3 Effects of salinity and sodicity on soil physicochemical attributes 50 3.4 Effect of salinity on plant growth 51 3.5 Plant responses to salinity 52 3.6 Microbe plant interaction 59

107

6. Regulation of low phosphate stress in plants Stanislaus Antony Ceasar

6.1 Introduction

v

123

vi

Contents

6.2 Morphological responses under low inorganic phosphate stress 124 6.3 Molecular responses to low phosphate stress 126 6.4 Role of arbuscular mycorrhizae fungal in low phosphate stress tolerance 139 6.5 Biochemical responses to low phosphate stress 141 6.6 Conclusion and future prospects 145 References 145

7. Regulation of flood stress in plants

9.5 Bioremediation 216 9.6 Phytoremediation 219 9.7 Genetic engineering and its application in the bioremediation of toxic metals 223 9.8 Conclusion 227 References 227 Further reading 235

10. Responses of plants to herbicides: Recent advances and future prospectives Suruchi Singh and Supriya Tiwari

Yoonha Kim, Raheem Shahzad and In-Jung Lee

7.1 Introduction 157 7.2 Plants strategies against flooding stress 159 7.3 Flooding tolerance mechanisms 162 7.4 Conclusion 169 Acknowledgment 169 References 170 Further reading 173

8. Heavy metals, water deficit, and their interaction in plants: an overview Mamta Hirve, Meeta Jain, Anshu Rastogi and Sunita Kataria

8.1 8.2 8.3 8.4

Introduction 175 Heavy-metal effects on plants 176 Water-deficit stress in plants 185 Combination of metal with water-deficit stress 188 8.5 Conclusions and future perspective 192 Acknowledgments 193 References 194 Further reading 206

9. Genetic engineering approaches and applicability for the bioremediation of metalloids Damanjeet Kaur, Ajay Singh, Abhijit Kumar and Saurabh Gupta

9.1 Introduction 207 9.2 Sources of metals 209 9.3 Metals: occurrence, speciation, and toxic effects 210 9.4 Remediation of toxic metals and metalloids 215

10.1 Introduction 237 10.2 Phenotypical manifestation 238 10.3 Herbicides: a multifaceted chemical 238 10.4 Physiological damage through generated reactive oxygen species intermediates 241 10.5 Direct damage to the physiological process 244 10.6 Chlorophyll and carotenoid biosynthesis 246 10.7 Conclusions 247 References 247

11. Effects of abiotic stresses on sugarcane plants with emphasis in those produced by wounds and prolonged post harvest periods Elena Sa´nchez-Elordi, Eva M. Dı´az, Roberto de Armas, Rocı´o Santiago, Borja Alarco´n, Carlos Vicente and Marı´a Estrella Legaz

11.1 11.2 11.3 11.4 11.5 11.6

Introduction 251 Heat and cold stress 252 Nutrition-related stresses 254 Salt stress 255 Drought 257 Stress produced by mechanical injuries 258 11.7 Sucrose synthesis and partitioning during abiotic stress 264 11.8 Conclusions and future prospects 266 References 267 Further reading 269

vii

Contents

12. Heavy metal stress and plant life: uptake mechanisms, toxicity, and alleviation Swati Singh, Vaishali Yadav, Namira Arif, Vijay Pratap Singh, Nawal Kishore Dubey, Naleeni Ramawat, Rajendra Prasad, Shivendra Sahi, Durgesh Kumar Tripathi and Devendra Kumar Chauhan

12.1 12.2 12.3 12.4

Introduction 271 Sources and metal bioavailability 275 Consequences of heavy metals in plants 276 Mechanisms of heavy metals uptake and transport in plants 277 12.5 Mechanism of heavy metals detoxification/ tolerance in plants 278 12.6 Avoidance mechanisms 278 12.7 Metal binding to cell wall 279 12.8 Tolerance mechanisms 280 References 282 Further reading 286

13. Nanoparticles in plants: morphophysiological, biochemical, and molecular responses Fabia´n Pe´rez-Labrada, Hipo´lito Herna´ndez-Herna´ndez, Mari Carmen Lo´pez-Pe´rez, Susana Gonza´lez-Morales, Adalberto Benavides-Mendoza and Antonio Jua´rez-Maldonado

13.1 Introduction 289 13.2 Nanotechnology and nanoparticles 290 13.3 Impacts of nanoparticles in plants 291 13.4 Conclusion 311 References 311

14. Regulations of reactive oxygen species in plants abiotic stress: an integrated overview Shiliang Liu and Rongjie Yang

14.1 Introduction 323 14.2 Reactive oxygen species regulation in plant organelles during abiotic stress 326 14.3 Antioxidants involved in stress-induced regulation of reactive oxygen species 333 14.4 Signaling roles of reactive oxygen species in plants under abiotic stress 339 14.5 Conclusion and future prospects 343 References 344 Further reading 353

15. Plant microbe interactions in plants and stress tolerance Hassan Etesami

15.1 Introduction 355 15.2 Salinity stress 358 15.3 Drought stress 364 15.4 Heavy metal toxicity stress 367 15.5 Mineral nutritional imbalance stress 373 15.6 Conclusions and future prospects 380 Acknowledgment 383 References 384

16. Phytohormonal signaling under abiotic stress Zahra Souri, Naser Karimi, Muhammad Ansar Farooq and Javaid Akhtar

16.1 16.2 16.3 16.4 16.5 16.6 16.7 16.8 16.9 16.10 16.11 16.12 16.13 16.14 16.15 16.16 16.17 16.18 16.19 16.20 16.21 16.22 16.23 16.24 16.25 16.26 16.27 16.28 16.29

Introduction 397 Abscisic acid 399 Abscisic acid biosynthesis 400 Abscisic acid signaling 402 Abscisic acid dependent signal transduction 402 Abscisic acid independent signal transduction 405 Auxin 406 Auxin biosynthesis 406 Auxin signaling 407 Brassinosteroids 409 Brassinosteroid biosynthesis 409 Brassinosteroids signaling 410 Ethylene 413 Ethylene biosynthesis 413 Ethylene signaling 413 Gibberellins 416 Gibberellin biosynthesis 417 Gibberellin signaling 418 Cytokinin 420 Cytokinins biosynthesis 420 Cytokinin signaling 421 Jasmonic acid and salicylic acid 423 Jasmonic acid biosynthesis 424 Salicylic acid biosynthesis 426 Jasmonic acid signaling 426 Salicylic acid signaling 428 Nitric oxide 429 NO biosynthesis 430 NO signaling 431

viii

Contents

16.30 16.31 16.32 16.33 16.34 16.35

Strigolactones 433 Strigolactone biosynthesis 434 Strigolactone signaling 434 Karrikins 436 Karrikin signaling 437 Cross talk between phytohormone signaling 437 Acknowledgment 443 References 443 Further reading 464

17. Role of sRNAs in abiotic stress tolerance Anuradha Patel, Sanjesh Tiwari, Madhulika Singh and Sheo Mohan Prasad

17.1 Introduction 467 17.2 sRNA 468 17.3 Biogenesis and mechanism of action of sRNAs 469 17.4 Mechanism of sRNA-mediated gene regulation 469 17.5 Role of mRNAs in stress tolerance 471 17.6 Role of small interfering RNAs in defense against pathogen 471 17.7 Role of sRNAs (lncRNAs—a type) in vernalization 472 17.8 Role of sRNAs in the development of leaf and leaf size and morphology 474 17.9 Role of sRNAs in alleviating salt stress 474 17.10 Role of sRNAs in oxidative stress regulation 475 17.11 Role of sRNAs in signaling of hormone 476 17.12 Conclusion 476 References 476 Further reading 480

18. Role of polyamines in plants abiotic stress tolerance: Advances and future prospects Chanda Bano, Nimisha Amist and N.B. Singh

18.1 Introduction 481 18.2 Synthesis of polyamines under abiotic stresses 482 18.3 Metabolism of polyamine during different stress conditions 483 18.4 Polyamines and abiotic stress tolerance in plants 485

18.5 Polyamine accumulating transgenic plants with improved abiotic stress tolerance 486 18.6 Polyamines role in response to different abiotic stresses 489 18.7 Polyamine treatment modulated plant-stress tolerance 490 18.8 Conclusion and future perspectives 491 References 492

19. The role of sugars in the regulation of environmental stress Nimisha Amist and N.B. Singh

19.1 Introduction References 508

497

20. Proteomics in relation to abiotic stress tolerance in plants Arti Gautam, Poonam Pandey and Akhilesh Kumar Pandey

20.1 Introduction 513 20.2 Understanding and identifying key metabolic proteins associated with abiotic stresses 514 20.3 Effect of reactive oxygen species on protein modification 517 20.4 Regulation of protein stability 525 20.5 Overexpression of organelle proteins in transgenic plants improves stress tolerance 529 20.6 Synthesis of the novel proteins 530 20.7 Conclusion and future aspects 531 References 531 Further reading 541

21. Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects Santwana Tiwari, Divya Gupta, Abreeq Fatima, Shikha Singh and Sheo Mohan Prasad

21.1 Introduction 543 21.2 Phytohormone biosynthesis and signaling pathways 544 21.3 Regulatory mechanism of phytohormones 556 21.4 Phytohormone-mediated modulation in plant under certain abiotic stresses 558 21.5 Future perspective 564 References 568

ix

Contents

22. Abiotic-stress tolerance in plants-system biology approach Poonam Pandey, Sarita Srivastava, Akhilesh Kumar Pandey and Rama Shanker Dubey

22.1 Introduction 577 22.2 Abiotic stresses and their impact on plant growth and metabolism 578 22.3 Systems biology approaches for improvement of plant’s abiotic-stress tolerance 581 22.4 Integration of multiple “omics” data 587 22.5 Modeling and simulation in plant system dynamics 589 22.6 Software and algorithms for plant systems biology 593 22.7 Conclusion and future prospects 595 References 599 Further reading 608

23. Plant single-cell biology and abiotic stress tolerance Mohsin Tanveer and Urwa Yousaf

23.1 Introduction 611 23.2 Single-cell models 612 23.3 Computational biology to study plant single-cell responses and abiotic stress tolerance 614 23.4 Techniques to study single-cell response to abiotic stress 615 23.5 Concluding remarks 620 References 621 Further reading 626

24. Nanoparticle application and abiotic-stress tolerance in plants Mohsin Tanveer, Babar Shahzad and Umair Ashraf

24.1 Introduction 627 24.2 Uptake, transportation, and translocation of nanoparticles 627 24.3 Nanoparticle application and its role in redox regulation 628 24.4 Nanoparticle application and photosynthetic apparatus 630 24.5 Nanoparticles application and ionic homeostasis 632 24.6 Nanoparticles toxicity in plants 633 24.7 Conclusion 636

References 636 Further reading 641

25. The role of aquaporins during plant abiotic stress responses Aditya Banerjee and Aryadeep Roychoudhury

25.1 Introduction 643 25.2 Brief history of aquaporins 644 25.3 Aquaporins: functional and structural significance in plants 644 25.4 Water dynamics and aquaporins 647 25.5 Roles of aquaporins in abiotic stresses 647 25.6 Conclusion and future perspectives 654 Acknowledgments 655 References 655

26. Tolerance mechanisms of medicinal plants to abiotic stresses Hamid Mohammadi, Saeid Hazrati and Mansour Ghorbanpour

26.1 The concept of increased resistance to abiotic stresses in medicinal plants 663 26.2 Tolerance to drought stress 664 26.3 Tolerance to salt stress 665 26.4 The mechanism of resistance to light stress and UV in medicinal plants 665 26.5 The resistance mechanism of medicinal and aromatic plants to temperature stress 668 26.6 Heat stress 669 26.7 Cold stress 671 26.8 Heavy metal stress 672 26.9 Conclusion 674 References 675 Further reading 679

27. Regulation of the Calvin cycle under abiotic stresses: an overview Sonika Sharma, Juhie Joshi, Sunita Kataria, Sandeep Kumar Verma, Soumya Chatterjee, Meeta Jain, Kratika Pathak, Anshu Rastogi and Marian Brestic

27.1 Introduction 681 27.2 Regulation of the Calvin cycle and its enzymes under abiotic stresses 686 27.3 Conclusion and future perspectives 703 Acknowledgments 704 References 704 Further reading 717

x

Contents

28. Roles of microRNAs in plant development and stress tolerance

31. Role of melatonin and serotonin in plant stress tolerance

Vaishali Yadav, Namira Arif, Vijay Pratap Singh, Rupesh Deshmukh, Shivendra Sahi, S.M. Shivaraj, Durgesh Kumar Tripathi and Devendra Kumar Chauhan

Muhammad Adil and Byoung Ryong Jeong

28.1 Introduction 719 28.2 Biogenesis of microRNAs 720 28.3 Role of microRNAs in plant growth and development 721 28.4 Role of microRNAs in various abiotic stresses 722 28.5 MicroRNAs and heavy-metal stress 723 28.6 MicroRNAs and oxidative stress 723 28.7 MicroRNAs and drought stress 724 28.8 MicroRNAs and salt stress 724 28.9 MicroRNAs and UV-B radiation 725 28.10 MicroRNAs and temperature stress 725 28.11 Conclusion and future outlook 726 References 729 Further reading 733

29. Nitric oxide under abiotic stress conditions Juan C. Begara-Morales, Mounira Chaki, Raquel Valderrama, Capilla Mata-Pe´rez, Marı´a N. Padilla-Serrano and Juan B. Barroso

29.1 Introduction 735 29.2 Nitric oxide sources under abiotic stress 736 29.3 Nitric oxide signaling under abiotic stress 739 29.4 Conclusion and perspectives 747 Acknowledgments 748 References 748

30. Role of metabolites in abiotic stress tolerance ´ gnes Szepesi A

30.1 Abiotic stress tolerance 755 30.2 Primary metabolites and osmoprotectants 755 30.3 Role of secondary metabolites: antioxidants and defense compounds 762 30.4 Conclusions and future prospects 763 Acknowledgments 765 References 765

31.1 Introduction 775 31.2 Tryptophan metabolism: biosynthesis of phyto-serotonin and melatonin 776 31.3 Fate of melatonin and serotonin in plants 778 31.4 Plant stress physiology and role of indolamines 779 31.5 Conclusion 786 References 786

32. Role of nitric oxide dependent posttranslational modifications of proteins under abiotic stress Mounira Chaki, Juan C. Begara-Morales, Raquel Valderrama, Capilla Mata-Pe´rez, Marı´a N. Padilla-Serrano and Juan B. Barroso

32.1 Introduction 793 32.2 Nitric oxide dependent posttranslational modification of proteins under abiotic stress 795 32.3 Conclusions and perspectives 803 References 803 Further reading 809

33. Regulatory role of circadian clocks in plant responses to abiotic stress Mohamed A. El-Esawi and Ibrahim M. Abdelsalam

33.1 Introduction 811 33.2 Role of the circadian clock in regulating plant stress responses 812 33.3 Circadian clock regulates stress-responsive genes 815 33.4 Abiotic stress affects clock genes transcription 816 33.5 Circadian clock mediates hormone signaling 817 References 819 Further reading 823

xi

Contents

34. Regulation of genes and transcriptional factors involved in plant responses to abiotic stress Mohamed A. El-Esawi

34.1 Introduction 825 34.2 Gene regulation and transcriptional factors in plant response to salt stress 826 34.3 Regulation of genes and transcriptional factors in plant response to drought stress 827 34.4 Heavy metal stress and its transcriptional factors regulation 828 34.5 Genes and transcriptional factors regulation of chilling and cold stress 829 34.6 Gene regulation of waterlogging tolerance 829 34.7 Transcriptional factors regulation of flooding stress 830 References 830 Further reading 833

35. Role of ionomics in plant abiotic stress tolerance Mohamed A. El-Esawi, Rajeshwar P. Sinha, Devendra Kumar Chauhan, Durgesh Kumar Tripathi and Jainendra Pathak

35.1 Introduction 835 35.2 Forward genetics and ionomic gene identification 836 35.3 Effect of heavy metal on plants 839 35.4 Toxicity of heavy metals in plants 840 35.5 Ionomics of heavy metals 841 35.6 Salt stress and plants 843 35.7 Role of osmolytes in plant protection 843 35.8 Ionomics of salt stress 845 35.9 Effect of osmotic stress on plants 846 35.10 Ionomics of osmotic stress 847 References 849 Further Reading 860

36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture Ved Prakash, Mohd Younus Khan, Padmaja Rai, Rajendra Prasad, Durgesh Kumar Tripathi and Shivesh Sharma

36.1 Introduction

861

36.2 Direct mechanism 865 36.3 Indirect mechanism 867 Conclusion 874 Acknowledgment 875 References 875 Further reading 882

37. Management of abiotic stress and sustainability Afaf M. Hamada and Youssef M. Hamada

37.1 Introduction 883 37.2 Economic effects of the most disturbed abiotic stress 884 37.3 Drought 884 37.4 Temperature 885 37.5 Flooding 887 37.6 Salinity 888 37.7 Greenhouse gas 889 37.8 Management of abiotic stress 889 37.9 Breeding 890 37.10 Fertilizers 890 37.11 Management of impacts of abiotic stress in southeast Mediterranean Sea 891 37.12 Mathematical model of future of sugar beet industry (FOSI) in North Egypt 897 37.13 Optimal solutions 899 References 905 Further reading 912 Appendix 912

38. Use of quantitative trait loci to develop stress tolerance in plants Dev Paudel, Smit Dhakal, Saroj Parajuli, Laxman Adhikari, Ze Peng, You Qian, Dipendra Shahi, Muhsin Avci, Shiva O. Makaju and Baskaran Kannan

38.1 Introduction 917 38.2 Types of abiotic stress in plants 918 38.3 Concluding remarks and future perspectives 943 References 945 Further reading 964

Index 967

List of contributors Ibrahim M. Abdelsalam Alnoor Laboratory, Qotour, Egypt Abhijit Kumar

Department of Biotechnology, Chandigarh University, Gharuan, India

Laxman Adhikari

Kansas State University, Manhattan, KS, United States

Muhammad Adil Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, Republic of Korea; H.E.J. Research Institute of Chemistry-Biotechnology Wing, International Center for Chemical and Biological Sciences, University of Karachi, Karachi, Pakistan Hamaad Raza Ahmad Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Javaid Akhtar Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Borja Alarco´n Team of Intercellular Communication in Plant Symbiosis, Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University, Madrid, Spain Mujahid Ali Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Shafaqat Ali Department of Environmental Sciences & Engineering, Government College University Faisalabad, Faisalabad, Pakistan Nimisha Amist Plant Physiology Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Namira Arif D D Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Umair Ashraf Department of Botany, University of Education (Lahore), Faisalabad-Campus, Faisalabad, Pakistan Muhsin Avci University of Florida, Gainesville, FL, United States Muhammad Ashar Ayub Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Aditya Banerjee

Department of Biotechnology, St. Xavier’s College (Autonomous), Kolkata, India

Chanda Bano Plant Physiology Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Juan B. Barroso Group of Biochemistry and Cell Signalling in Nitric Oxide, Department of Experimental Biology, Faculty of Experimental Sciences, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jae´n, Campus Universitario “Las Lagunillas” s/n, Jae´n, Spain Juan C. Begara-Morales Group of Biochemistry and Cell Signalling in Nitric Oxide, Department of Experimental Biology, Faculty of Experimental Sciences, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jae´n, Campus Universitario “Las Lagunillas” s/n, Jae´n, Spain Adalberto Benavides-Mendoza Department of Horticulture, Autonomous Agrarian University Antonio Narro, Saltillo, Mexico

xiii

xiv

List of contributors

Marian Brestic Republic

Department of Plant Physiology, Slovak University of Agriculture, Nitra, Slovak

Stanislaus Antony Ceasar Division of Plant Biotechnology, Entomology Research Institute, Loyola College, Chennai, India; Functional Genomics and Plant Molecular Imaging Lab, University of Liege, Liege, Belgium Aslıhan C ¸ etinba¸s-Genc¸ Science and Arts Faculty, Department of Biology, Marmara University, Go¨ztepe Campus, Istanbul, Turkey Mounira Chaki Group of Biochemistry and Cell Signalling in Nitric Oxide, Department of Experimental Biology, Faculty of Experimental Sciences, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jae´n, Campus Universitario “Las Lagunillas” s/n, Jae´n, Spain Soumya Chatterjee

Defence Research Laboratory, Tezpur, India

Devendra Kumar Chauhan D D Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Roberto de Armas Cuba

Department of Plant Biology, Faculty of Sciences, Havana University, Havana,

Rupesh Deshmukh National Agri-Food Biotechnology Institute (NABI), Mohali, India Smit Dhakal

University of Illinois-Urbana Champaign, Urbana, IL, United States

Eva M. Dı´az Team of Intercellular Communication in Plant Symbiosis, Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University, Madrid, Spain Nawal Kishore Dubey India

Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi,

Rama Shanker Dubey Department of Biochemistry, Institute of Science, Banaras Hindu University, Varanasi, India Mohamed A. El-Esawi

Botany Department, Faculty of Science, Tanta University, Tanta, Egypt

Hassan Etesami Faculty of Agricultural Engineering & Technology, Department of Soil Science, Agriculture & Natural Resources Campus, University of Tehran, Tehran, Iran Muhammad Ansar Farooq Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Zia Ur Rahman Farooqi Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Abreeq Fatima Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Arti Gautam Department of Biochemistry, Institute of Science, Banaras Hindu University, Varanasi, India Mansour Ghorbanpour Department of Medicinal Plants, Faculty of Agriculture and Natural Resources, Arak University, Arak, Iran Susana Gonza´lez-Morales CONACyT-Department University Antonio Narro, Saltillo, Mexico

of

Horticulture,

Autonomous

Agrarian

Divya Gupta Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Saurabh Gupta

Department of Microbiology, Mata Gujri College, Fatehgarh Sahib, India

Afaf M. Hamada Botany and Microbiology Department, Faculty of Science, Assiut University, Assiut, Egypt

List of contributors

xv

Youssef M. Hamada Water and Land Economics Researches Department, Agricultural Economics Research Institute, Agriculture Research Center, Giza, Egypt Saeid Hazrati Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran Hipo´lito Herna´ndez-Herna´ndez Meeta Jain

Papaloapan University, Loma Bonita, Oaxaca, Mexico

School of Biochemistry, Devi Ahilya University, Indore, India

Mamta Hirve

School of Biochemistry, Devi Ahilya University, Indore, India

Byoung Ryong Jeong Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, Republic of Korea; Department of Horticulture, Division of Applied Life Science Graduate School (BK 21 Plus program), Gyeongsang National University, Jinju, Republic of Korea; Research Institute of Life Science, Gyeongsang National University, Jinju, Republic of Korea Juhie Joshi Canada

Plant Science Department, Macdonald Campus, McGill University, Montreal, QC,

Antonio Jua´rez-Maldonado Narro, Saltillo, Mexico

Department of Botany, Autonomous Agrarian University Antonio

Baskaran Kannan University of Florida, Gainesville, FL, United States Naser Karimi Laboratory of Plant Physiology, Department of Biology, Faculty of Science, Razi University, Kermanshah, Iran Sunita Kataria

School of Biochemistry, Devi Ahilya University, Indore, India

Damanjeet Kaur Department of Microbiology, Mata Gujri College, Fatehgarh Sahib, India; Department of Biotechnology, Punjabi University, Patiala, India Hinnan Khalid Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Mohd Younus Khan Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India Yoonha Kim Division of Plant Biosciences, School of Applied Biosciences, Kyungpook National University, Daegu, South Korea In-Jung Lee Division of Plant Biosciences, School of Applied Biosciences, Kyungpook National University, Daegu, South Korea Marı´a Estrella Legaz Team of Intercellular Communication in Plant Symbiosis, Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University, Madrid, Spain Shiliang Liu College of Landscape Architecture, Sichuan Agricultural University, Chengdu, P.R. China Mari Carmen Lo´pez-Pe´rez Department of Horticulture, Autonomous Agrarian University Antonio Narro, Saltillo, Mexico Shiva O. Makaju University of Georgia, Athens, GA, United States Capilla Mata-Pe´rez Group of Biochemistry and Cell Signalling in Nitric Oxide, Department of Experimental Biology, Faculty of Experimental Sciences, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jae´n, Campus Universitario “Las Lagunillas” s/n, Jae´n, Spain Hamid Mohammadi

Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran

Komal Naz Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan

xvi

List of contributors

Marı´a N. Padilla-Serrano Group of Biochemistry and Cell Signalling in Nitric Oxide, Department of Experimental Biology, Faculty of Experimental Sciences, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jae´n, Campus Universitario “Las Lagunillas” s/n, Jae´n, Spain Akhilesh Kumar Pandey Department of Biochemistry, Institute of Science, Banaras Hindu University, Varanasi, India Poonam Pandey Department of Biochemistry, Institute of Science, Banaras Hindu University, Varanasi, India Saroj Parajuli

University of Florida, Gainesville, FL, United States

Anuradha Patel Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Jainendra Pathak Laboratory of Photobiology and Molecular Microbiology, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, India; Department of Botany, Pt. Jawaharlal Nehru College, Banda, India Kratika Pathak

School of Biochemistry, Devi Ahilya University, Indore, India

Dev Paudel University of Florida, Gainesville, FL, United States Ze Peng

University of Florida, Gainesville, FL, United States

Fabia´n Pe´rez-Labrada Department of Horticulture, Autonomous Agrarian University Antonio Narro, Saltillo, Mexico Ved Prakash Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India Rajendra Prasad Department of Horticulture, Kulbhaskar Ashram Post Graduate College, Prayagraj, India Sheo Mohan Prasad Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India You Qian

University of Florida, Gainesville, FL, United States

Padmaja Rai Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India Naleeni Ramawat India

Amity Institute of Organic Agriculture, Amity University Uttar Pradesh, Noida,

Anshu Rastogi Laboratory of Bioclimatology, Department of Ecology and Environmental ´ Poland Protection, Poznan University of Life Sciences, Poznan, Muhammad Rizwan Department of Environmental Sciences & Engineering, Government College University Faisalabad, Faisalabad, Pakistan Aryadeep Roychoudhury Kolkata, India

Department of Biotechnology, St. Xavier’s College (Autonomous),

Shivendra Sahi University of the Sciences in Philadelphia (USP), Philadelphia, PA, United States Elena Sa´nchez-Elordi Team of Intercellular Communication in Plant Symbiosis, Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University, Madrid, Spain Rocı´o Santiago Team of Intercellular Communication in Plant Symbiosis, Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University, Madrid, Spain Dipendra Shahi University of Florida, Gainesville, FL, United States

List of contributors

Babar Shahzad

xvii

School of Land and Food, University of Tasmania, Hobart, Australia

Raheem Shahzad Division of Plant Biosciences, School of Applied Biosciences, Kyungpook National University, Daegu, South Korea Shivesh Sharma Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India Sonika Sharma

Defence Research Laboratory, Tezpur, India

S.M. Shivaraj Laval University, Quebec City, QC, Canada; National Research Centre on Plant Biotechnology, New Delhi, India Ajay Singh

Department of Food Technology, Mata Gujri College, Fatehgarh Sahib, India

Madhulika Singh Centre of Advance Studies, Department of Botany, Banaras Hindu University, Varanasi, India N.B. Singh Plant Physiology Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Shikha Singh Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Suruchi Singh India

Department of Botany, Institute of Science, Banaras Hindu University, Varanasi,

Swati Singh D D Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Vijay Pratap Singh Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, India Rajeshwar P. Sinha Laboratory of Photobiology and Molecular Microbiology, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, India Muhammad Irfan Sohail Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Zahra Souri Laboratory of Plant Physiology, Department of Biology, Faculty of Science, Razi University, Kermanshah, Iran Sarita Srivastava Department of Biochemistry, Institute of Science, Banaras Hindu University, Varanasi, India ´ gnes Szepesi Department of Plant Biology, Institute of Biology, University of Szeged, Szeged, A Hungary Mohsin Tanveer

School of Land and Food, University of Tasmania, Hobart, Australia

Sanjesh Tiwari Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Santwana Tiwari Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Supriya Tiwari India

Department of Botany, Institute of Science, Banaras Hindu University, Varanasi,

Durgesh Kumar Tripathi Noida, India

Amity Institute of Organic Agriculture, Amity University Uttar Pradesh,

Muhammad Usman Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan

xviii

List of contributors

Raquel Valderrama Group of Biochemistry and Cell Signalling in Nitric Oxide, Department of Experimental Biology, Faculty of Experimental Sciences, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jae´n, Campus Universitario “Las Lagunillas” s/n, Jae´n, Spain Filiz Vardar Science and Arts Faculty, Department of Biology, Marmara University, Go¨ztepe Campus, Istanbul, Turkey Sandeep Kumar Verma

Institute of Biological Science, SAGE University, Indore, India

Carlos Vicente Team of Intercellular Communication in Plant Symbiosis, Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University, Madrid, Spain Aisha A. Waris Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan Vaishali Yadav D D Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Prayagraj, India Rongjie Yang China

College of Landscape Architecture, Sichuan Agricultural University, Chengdu, P.R.

Fatma Yanık Science and Arts Faculty, Department of Biology, Marmara University, Go¨ztepe Campus, Istanbul, Turkey Urwa Yousaf Pakistan

Department of Computer Sciences, University of Agriculture Faisalabad, Faisalabad,

Muhammad Zia ur Rehman Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan

C H A P T E R

1 Abiotic stress induced programmed cell death in plants Fatma Yanık, Aslıhan C ¸ etinba¸s-Genc¸ and Filiz Vardar Science and Arts Faculty, Department of Biology, Marmara University, Go¨ztepe Campus, Istanbul, Turkey

1.1 Introduction All organisms should cope with numerous environmental stress factors during their life span by activating their endogenous defensive strategies. In the course of evolution, due to immobile nature of plants, they have developed adaptive processes to some extent to stress conditions. Plants face both biotic (bacteria, fungi, and virus attack) and abiotic [extreme temperatures, drought, flooding, high salinity, pesticides, heavy metals, excessive light, and ultraviolet (UV) radiation] stresses at various stages of their development (Bostock et al., 2014; Petrov et al., 2015). Recently, it has come forward that plant cells can no longer maintain homeostasis according to the failure of metabolic pathway upon a certain threshold of stress factors, and they initiate self-defense program that is aimed at the selective death of the cells. Such selective programmed cell death (PCD) ultimately provides survival benefits for the whole plant under stressful conditions (Drew et al., 2000; Tuzhikov et al., 2011). PCD has been described as genetically controlled and coordinated elimination process of selected cells with specific enzymatic (proteases and nucleases) cascade. PCD, as a wellorganized cell suicide process, is characterized with the breakdown of the cell through condensation, vacuolization, shrinkage, and fragmentation of both cytoplasm and nucleus ´ ´ (Wituszynska and Karpinski, 2013; Petrov et al., 2015; Nath and Lu, 2015). Plant PCD is classified into two broad groups: developmentally regulated (dPCD) and environmentally induced (ePCD) (Olvera-Carrillo et al., 2015). Developmentally occurred PCD is presented in Table 1.1, both in vegetative and reproductive organs. Besides, ePCD appears in response to pathogen attack (Greenberg, 1997), high low temperature (Lord and Gunawardena, 2011), UV (Ferreyra et al., 2016), flooding (Chen et al., 2014), salinity

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00015-1

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© 2020 Elsevier Inc. All rights reserved.

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1. Abiotic stress induced programmed cell death in plants

TABLE 1.1 Developmentally occurred programmed cell death (PCD) in vegetative and generative organs.

Vegetative organ development

Reproductive organ development

Tissues and cells undergo PCD

References

Tracheary element differentiation

Fukuda (2000)

Root cap cells

Wang et al. (1996a)

Aerenchyma formation

Rantong and Gunawardena (2015)

Leaf abscission

Bar-Dror et al. (2011)

Leaf senescence

Lim et al. (2007)

Leaf morphogenesis

Gunawardena et al. (2007)

Trichome development

Papini et al. (2010)

Sex determination

Dellaporta and Calderon-Urrea (1994)

Nonfunctional megaspore degeneration

Bell (1996)

Synergids and antipodals

An and You (2004)

Pollen incompatibility

Kacprzyk et al. (2011)

Stylar transmitting tissue

Cheung (1996)

Nucellus

Li et al. (2003)

Endosperm

Wei et al. (2002)

Aleurone cells

Wang et al. (1996b)

Suspensor

Wredle et al. (2001)

Anther tapetum

¨ nal (2012) Vardar and U

Anther connective tissue and filament

¨ nal (2011) Vardar and U

Flower abscission

Bar-Dror et al. (2011)

(Monetti et al., 2014), drought (Hameed et al., 2013), heavy metal (Vardar et al., 2016), and newly arising nanoparticles (NPs) (Yanık et al., 2017). It has been considered that plants have evolved their own pathways due to the presence of cell walls that prevent the dying cells from being phagocytosed by neighboring cells as it is in animals. Besides, very few conserved regulatory proteins or protein domains have been classified at the molecular level among eukaryotic PCD forms (Danon et al., 2004). Moreover, most of the PCD regulators and genes are evolutionarily conserved within the plant kingdom. Although there are some morphological and biochemical similarities between dPCD and ePCD, such as vacuolar processing enzyme (VPE) activity, reactive oxygen species (ROS) generation, and calcium (Ca21) signaling (Huysmans et al., 2017), it has been indicated that transcriptional signatures of dPCD and ePCD are largely distinct from each other (Olvera-Carrillo et al., 2015).

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1.2 Relation between reactive oxygen species and programmed cell death

3

Plant cells are regulated by endogenous factors, such as plant growth regulators (e.g., salicylic and jasmonic acids and ethylene) under environmental stress factors. These endogenous factors also inspect the production of ROS and cause the emergence of other signaling molecules proceeding PCD (Nath and Lu, 2015). It has been known that lower doses of ROS are assigned as a secondary signaling molecule that mediates the responses toward stress. But at higher concentrations, they cause oxidative stress that may result in damage to macromolecules, such as proteins, lipids, DNA, and RNA, leading to cell death (Woo et al., 2013; Coll et al., 2014; Petrov et al., 2015). Although there are a lot of researches on PCD, the relation between induced abiotic stress and PCD is still unclear and remains to be investigated at the molecular level. In the present review, recent advancements on abiotic stress induced PCD are summarized.

1.2 Relation between reactive oxygen species and programmed cell death Triplet oxygen, being as a free radical with two impaired electrons, can react with molecules to form ROS that are highly reactive and toxic
(Gill and Tuteja, •2010). The 2 , hydroxyl radical ( OH), and most occurring free radicals are superoxide anion O 2
perhydroxyl radical HO2 . Besides, hydrogen peroxide (H2O2) and singlet oxygen (1O2) are also described as nonradicals. Free and nonradicals are produced as byproducts of aerobic and photosynthetic reactions during several metabolic processes in chloroplasts, mitochondria, and peroxisomes (Sharma et al., 2012). ROS are also produced in the cell wall, apoplast, and plasma membrane during the enzymatic activities of NADPH oxidase, peroxidase, and amine oxidase, respectively (Reape et al., 2015; Caverzan et al., 2016). Although lower/optimal doses of ROS act as signaling molecules mediating diverse biological processes, the higher concentrations generate a significant threat leading to oxidative stress and PCD eventually (Coll et al., 2014; Petrov et al., 2015). Under steady conditions, ROS are scavenged in plant cells by antioxidant defense system providing equilibrium/balance between production and eliminating of ROS. The antioxidant defense system (Fig. 1.1) consists of several enzymatic and nonenzymatic antioxidants. The most experienced enzymatic antioxidants are peroxidases (ascorbate, glutathione, and guaiacol), superoxide dismutase, catalase, reductases (dehydroascorbate, glutathione, and monodehydroascorbate), and glutathione S-transferase. Furthermore, nonenzymatic antioxidants include phenolic compounds, carotenoids, ascorbic acid, alkaloids, glutathione, oxidized glutathione, and α-tocopherols antioxidants (Gill and Tuteja, 2010). Plants face exogenous and endogenous stresses during their consecutive stages of development including senescence. The balance between production and scavenging of ROS may be disturbed by various types of environmental factors. Due to these perturbations, intracellular ROS levels rise rapidly. Overaccumulation of ROS under abiotic stresses alters cellular functions unfavorably by damaging nucleic acids, oxidizing proteins and lipids, and eventually causing PCD (Gill and Tuteja, 2010; Woo et al., 2013; Nath and Lu, 2015). ROS-related molecular signaling pathway in plants is still unclear, due to opposite act under environmental stresses. It has been known that the intracellular ROS level increases

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1. Abiotic stress induced programmed cell death in plants

a dri on ch ito

)

H2O

,m

X lact APhlorop

O2•−

Cu/Zn SOD

Hydrogen

Mn SOD

H2 O2

(cytosol)

Superoxide

(mitochondria)

(cy

ol, tos

Fento nr e

,c me iso

CATALASE

(cy

ol,

pe

rox is

om

Fe2+

e, c

OH•

Lipids peroxides

O2

GP

hlo

X

rop

lac

t, m ito

ch

Fe3+

Hydroxyle radical

2H2O +

tos

pero i d e x n tio ac

rox pe

on

dri a)

H2O

GST

(mitochondria, cytosol, membrane)

Detoxified Lipids

FIGURE 1.1 SOD, APX, GPX, and GST are the fundamental antioxidant defense enzymes against ROS. APX, Ascorbate peroxidase; GPX, glutathione peroxidase; GST, glutathione S-transferase; ROS, reactive oxygen species; SOD, superoxide dismutase. Source: Modified from Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48 (12), 909 930.

according to suppression of scavenging enzyme activities. This situation might result from the action of different plant growth regulators and cross talk between different signaling pathways. Another possibility might originate from differences in the ROS locations, where they are produced and/or accumulated during different stresses (Apel and Hirt, 2004; Pitzschke et al., 2006). Although ROS are considered as toxic products, spatial and temporal alterations of ROS levels act as initial signal necessary for growth, development, stress tolerance, and PCD (Apel and Hirt, 2004; Gechev et al., 2006). It has been known that altered ROS levels may change the sensitivity of the cellular response due to previous exposure to stress, chemical identity, concentration, production site, duration of action, plant developmental stage, and interaction with other signaling molecules, such as nitric oxide (NO), lipid messengers, and plant growth regulators (Zaninotto et al., 2006; Kwak et al., 2006). Under abiotic stress conditions, signaling molecules are often generated from chloroplasts, mitochondria, and/or the endoplasmic reticulum (ER). These signals cause metabolic imbalances and ROS accumulation, which are reacted and transmitted to inner side of the cell, and in consequence, physiological and biochemical reactions are rearranged to adapt the environmental alterations (Suzuki et al., 2012; Petrov et al., 2015). It has been known that the mobility and interaction with diverse cellular compartments affect the spa• tial control of ROS generation. Because of their electrical charge, 1O2, O2 2 , and OH are almost immobile, but H2O2 can cross biological membranes with a quite distance from its

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1.2 Relation between reactive oxygen species and programmed cell death

5

production site. H2O2 needs special aquaporins called peroxoporins for their transports because membranes are nearly impermeable to H2O2 (Bienert et al., 2006; Gechev et al., 2006). Transport of H2O2 provides the adjustment of local concentrations. Its mobility causes increased levels of H2O2, which leads to inhibition of the chloroplastic antioxidants, such as ascorbate peroxidase (APX) (Davletova et al., 2005). It has been thought that along with diffusion of extracellular ROS, NO and salicylic acid (SA) also penetrate into the cell. The SA and NO downregulate the scavenging antioxidants APX and CAT culminating in more production and accumulation of ROS and leading to the activation of PCD process (Gadjev et al., 2008). Under stress conditions, ROS triggers the oxidation of cardiolipins and weakens the stability of cytochrome c (cyt c) locating in the inner mitochondrial membrane causing its diffusion into the intramembrane region. Meanwhile, ROS triggers the mobilization of Ca21 ions from the ER lumen to mitochondria. Ca21 ions as secondary signaling molecules induce to decrease of mitochondrial membrane potential (ΔΨm) and open the mitochondrial permeability transition pores (MPTP) in the outer mitochondrial membrane allowing cyt c extrusion to the cytoplasm (Ott et al., 2007; Williams et al., 2014). It has been proposed that extrusion of cyt c provokes more ROS generation in the mitochondria, forming a positive feedback to enhance the initial signal. In combination with ROS, cyt c release appears to be one of the prerequisites for PCD execution more than the direct activation (Vacca et al., 2006; Reape and McCabe, 2008). Researchers suggested that plant proteases responsible for caspase-like activities are upstream of ROS production and cyt c release (Gunawardena and McCabe, 2015). It has been widely known that ROS signal transduction has an indispensable role during PCD, development, growth, and stress regulation. Several studies have revealed that signaling pathways of mitogen-activated protein kinase (MAPK) are both promoted and regulated by ROS production via unknown ROS sensors. MAPKs are serine/threonine kinases and fundamentally consist of MAP kinase kinase kinases (MAP3Ks/MAPKKKs/MEKKs), MAP kinase kinases (MAP2Ks/MAPKKs/MEKs/MKKs), and MAP kinases (MAPKs/ MPKs). Under stress conditions, each subgroup of MAPK activation is induced by a cascade of sequential phosphorylation events. Phosphorylation-mediated signal transduction begins with the activation of MAPKKK, which, in turn, phosphorylates and activates a specific MAPKK and MAPK (Mishra et al., 2006; Pitzschke and Hirt, 2009; Rodriguez et al., 2010; Sinha et al., 2011). Besides, MAPK cascade is mediated by different types of scaffold proteins for their formation and integrity. It has been revealed that Arabidopsis (Arabidopsis thaliana) genome includes more than 80 MAPKKKs, 10 MAPKKs, and 20 MAPKs, which are related to the type of environmental stress and developmental stage attached to different MAPK modules (Pitzschke and Hirt, 2009). MAPKs have an important role in the consecutive transduction of signals between plasma membrane and nucleus phosphorylating a wide range of substrates, such as other kinases or transcription factors culminating in gene expression, cell proliferation, cell survival, and death (Son et al., 2011). Although certain ROS receptors are still unknown, it has been known that receptorlike/pelle kinases (RLKs), which are serine threonine protein kinases, play a crucial role in plant stress response. RLKs perceive signals by an extracellular ligand-binding domain and transmit down to effector genes. Specifically, cysteine-rich RLKs (CRKs) play the critical role in plant PCD. It has been reported that in Arabidopsis

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1. Abiotic stress induced programmed cell death in plants

oxidative stress, pathogen attack and SA stimulate the transcription of CRKs (Shiu and Bleecker, 2001, 2003; Shiu et al., 2004).

1.3 Programmed cell death related proteases Proteases that mediate cell death degrade the cellular components by initiating, enhancing, or altering the morphology, biochemistry, and physiology of the cell. Proteases are divided into six different catalytic families: serine, cysteine, aspartic, threonine, glutamic, and metallopeptidases. In animal systems, most of the morphological and biochemical symptoms of apoptosis are related to caspase activity. Caspases are known as cysteinedependent aspartic acid (Asp) specific proteases cleaving their substrates after an Asp residue in P1 position, which are essential regulators of PCD in animal systems (Cai et al., 2014). Although there are no caspase orthologs in plant genomes, caspase-related proteins and caspase-like activities (Table 1.2) were observed in plants in the last decades (Rocha et al., 2017). Various experimental systems, such as using synthetic caspase-1 substrate YVAD (Tyr-Val-Ala-Asp), have succeeded to reveal and measure caspase-like activities in plant systems (Rotari et al., 2001; McStay et al., 2007). Recently, it has been identified that plant metacaspases are distant relatives of animal caspases (Uren et al., 2000). Metacaspases prefer to cleave their substrates following basic residues arginine (Arg) or lysine (Lys), rather than Asp (Watanabe and Lam, 2005; He et al., 2008; Salvesen et al., 2016). It has been clearly revealed that metacaspases as being cysteine-dependent proteinases do not have a caspase-like enzymatic activity due to not being able to cleave synthetic caspase substrates and not being blocked by caspase inhibitors (Vercammen et al., 2004; He et al., 2008; Tsiatsiani et al., 2011). Metacaspases generally appear in the cytosol, but while PCD occurs, they can change location to the other organelles (Woltering, 2004; Bozhkov et al., 2005). Activation of metacaspase precursors requires increased levels of Ca21 or an alkali pH of 7 8.5 (He et al., 2008; Tsiatsiani et al., 2011). Plant metacaspases have been classified as types I and II. In type I, they have an Nterminal prodomain being like initiator procaspases and in type II, there is a lack of the prodomain having a long linker between the p20 and p10 chains of the catalytic domain. TABLE 1.2 Plant proteases involved in programmed cell death. Protease

Protease family

Preferred substrate

Preferred synthetic caspase substrate

Metacaspase

Cysteine protease

Arg, Lys

VPE (legumain)

Cysteine protease

Asn

YVAD (caspase-1 substrate)

Phytaspase

Serine protease

Asp

VEID (caspase-6 substrate)

Saspase

Serine protease

Asp

IETD (caspase-8 substrate) VEHD, VKMD, VNLD (caspase-6 substrates)

26S proteasome ß subunit 1

Threonine protease

Asp, Glu

DEVD (caspase-3 substrate)

Arg, Arginine; Asn, asparagine; Asp, aspartic acid; Lys, lysine; VPE, vacuolar processing enzyme.

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1.3 Programmed cell death related proteases

7

Type II metacaspases are similar to executioner procaspases (Lord and Gunawardena, 2012; Choi and Berges, 2013; Salvesen et al., 2016). Metacaspases act functionally during developmental and stress-induced cell death. It has been revealed that Arabidopsis encodes three type I (AtMC1, AtMC2, and AtMC3) and six type II (AtMC4, AtMC5, AtMC6, AtMC7, AtMC8, and AtMC9) metacaspases. Regarding oxidative stress and pathogen attack, AtMC4 acts as a positive regulator. Besides, the highly homologous AtMC1 and AtMC2 function antagonistically during hypersensitive response (Coll et al., 2014; Salvesen et al., 2016). Moreover, AtMC8 has a role of UV- and H2O2-induced PCD as a positive regulator (He et al., 2008). Furthermore, AtMC9 performed during xylem formation contributing the cleaning of the cytosolic remnants in dying cells (Bollhoner et al., 2013). Until now several proteases have been associated with caspase-like activities. They are categorized into two broad groups: subtilisin-like serine proteases (saspases and phytas¨ nal, 2008; Vartapetian et al., 2011). pases) and cysteine proteases (VPEs) (Vardar and U VPEs, also known as legumains, are cysteine proteases similar to animal caspases and plant metacaspases (Hatsugai et al., 2004; Cai et al., 2014). Although VPEs prefer to cleave their substrates after an asparagine residue, they also recognize and cleave the caspase-1 substrate YVAD. Besides synthetic caspase-1, inhibitor ac-YVAD-CHO blocks activation of VPE (Sexton et al., 2007; Misas-Villamil et al., 2013). Synthesis of VPEs is an inactive proprotein precursor; initially, once synthesized, VPEs include a signal peptide sequence that addresses them to the vacuole. During translation in the ER, the signal peptide is excised creating another inactive form of proVPE containing N-terminal propeptide, active domain, and a C-terminal inhibitory propeptide (Kuroyanagi et al., 2002; Hara-Nishimura et al., 2005). While proVPE is transported to the vacuole, C-terminal inhibitory propeptide is removed by self-autocatalysis due to acidic pH (B5.5). As a result the production of an active intermediate isoform of VPE is completed (Misas-Villamil et al., 2013; Rantong and Gunawardena, 2015). Further experiments suggested that VPEs act as regulators of ER stress, abiotic stress, hypersensitive response, leaf senescence, lateral root formation, seed development, and male female embryogenesis (Kuriyama and Fukuda, 2002; Lam, 2004; van Doorn and Woltering, 2005; Gunawardena and McCabe, 2015). Phytaspase is a plant Asp-specific protease and categorized as a subtilisin-like serine protease (Vartapetian et al., 2011). It also exhibits caspase-like activities and cleaves synthetic caspase-6 substrate VEID, preferentially. Besides, it can also cleave caspase-1 (YVAD), -9 (LEHD), -8 (IETD), and -2 (VDVAD) substrates, but they have no affinity to caspase-3 (DEVD) substrate. Phytaspase was shown to mediate PCD, triggered by biotic and abiotic stresses (Chichkova et al., 2010). Phytaspases are located in the extracellular fluid as inactive zymogens. During maturation, their N-terminal signal peptide and prodomain are cut out, leaving behind the protease domain. After maturation process, they enter the cell during cell death. It has been also reported that ROS accumulation and cyt c release are increased according to the overexpression of the phytaspases during PCD. Besides, downregulation of phytaspases suppresses the tobacco mosaic virus (TMV)induced PCD (Chichkova et al., 2010; Vartapetian et al., 2011). Saspases are also subtilisin-like serine-dependent proteases with an Asp cleavage site. They are synthesized as inactive enzyme precursors (preprosaspases), as it happened in phytaspases (Rautengarten et al., 2005; Tripathi and Sowdhamini, 2006; Vartapetian et al., 2011). After cleavage of the signal peptide and a prodomain the saspase precursor

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1. Abiotic stress induced programmed cell death in plants

becomes mature with their peptidase domain (Vartapetian et al., 2011). Saspase activity is observed both in the extracellular fluid (apoplast) and cytoplasm during plant PCD. Saspases exhibit enzymatic activity against synthetic caspase-8 substrate (IETD) and caspase-6 substrates (VEHD, VKMD, and VNLD), but they do not show peptidase activity to caspase 1 (YVAD), caspase 2 (VDVAD), caspase 3 (DEVD), caspase 4 (LEVD), caspase 5 (WEHD), and caspase 6 (VEID) (Coffeen and Wolpert, 2004; Vartapetian et al., 2011). Although the functions of saspases remain unclear, it has been revealed that saspases regulate proteolytic degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) during biotic and abiotic PCD (Vartapetian et al., 2011). Recently, caspase-3-like activities were detected during plant PCD. It has been revealed that 26S proteasome β subunit 1 (PBA1) is responsible for display DEVDase (caspase-3like) activity during hypersensitive response (Hatsugai et al., 2009). The 26S proteasome is a protease complex, and the core unit is the 20S proteasome consisting α and β subunits. According to the reports, hypersensitive response was inhibited caspase-3 and proteasome inhibitors proving the caspase-3-like activities of the 26S proteasome. Similarly, inhibition of 26S proteasome prevented tracheal element differentiation (Woffenden et al., 1998). Besides, blocking proteasome activity reduces the degradation of misfolded proteins, causing ER stress induced PCD. These results support that PBA1 has caspase-like activities in plants (Kisselev et al., 2003; Cai et al., 2014).

1.4 Abiotic stress and programmed cell death Stress is an unfavorable external factor that can potentially limit plant growth and reproduction. These stress factors can be defined in two categories as biotic and abiotic stresses. Biotic stress factors include pests and pathogens, such as fungi, bacteria, viruses, nematodes, and herbivorous insects. Abiotic stress factors arise from chilling, high temperature, drought, flooding, salinity, UV radiation heavy metals, NPs, etc. Organisms that are affected by stress can develop tolerance, resistance, or avoidance mechanisms for their survival. Because of being sessile organisms, plants cannot avoid physically by external stress factors and face to various types of stress factors (Madlung and Comai, 2004). Plants have significant defense strategies to cope with environmental stress factors. A widespread feature of plant response against abiotic stresses is the production of ROS that are primary regulators of signaling pathways on plant defense. Excess ROS accumulation causes some cellular defects, such as DNA damage, lipid peroxidation, and protein oxidation (Petrov et al., 2015). Plants have antioxidant defense mechanisms consisting enzymatic and nonenzymatic systems as previously mentioned. The antioxidant system determines the equilibrium between ROS production and scavenging. The ROS amount increases when the balance disrupts under abiotic stress conditions, and the antioxidant system overcomes by oxidative stress. It has been known that lower concentrations of ROS play as a secondary messenger that mediates stress response, and the higher concentrations cause damage that finally induces to PCD (Huysmans et al., 2017). High concentrations of ROS damage the biomolecules and lead to PCD by upregulation of caspase-like activities (Reape and McCabe, 2008).

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Although abiotic stress induced PCDs are of considerable interest in the context of applied agriculture, ecology, and environmental protection, there are still unclear steps in our understanding of ROS PCD relation as well as the specific protease activation. It should be also considered that when plants are subjected to a combination of multiple stresses, they respond in a different manner in comparison with a single type of stress.

1.4.1 High and low temperature induced programmed cell death Plants experience different temperature conditions throughout their life cycles due to climatic changes. Every plant has a specific optimal temperature at which plant growth progresses at the maximum rate (Hatfield and Prueger, 2015). If the environmental temperature is less than or more than the optimal temperature, it alters the plant growth and reproduction. The global air temperature has been expected to increase by 0.2 C every year, and current temperature has been expected to rise by 4 C until 2100 (Intergovernmental Panel on Climate, 2007). Increasing temperature with the global climate change poses a threat to agricultural productivity all over the world. High temperature is one of the environmental stress factors, limiting the production of many cultivated plants. The effects of high temperature differ due to the plant species, growth stage, temperature degree, exposure duration, and susceptible tissue and/or organs (Sung et al., 2003; Larkindale et al., 2005). According to the experiences, high-temperature stress resulted in inhibition of seed germination, reduction of plant growth, water loss, photosynthetic alterations, yield loss, reduction of crop quality, and oxidative stress due to excess ROS production (Hasanuzzaman et al., 2013). Particularly in extreme temperatures, the damage of cellular organization and ROS generation occurs immediately leading to PCD (Qi et al., 2010). High temperature induced PCD was described by several studies in higher plants (Table 1.3). The high temperature during the flower development of Vigna unguiculata causes early degeneration of tapetum leading to male sterility (Ahmed et al., 1992). Similarly, high temperature induced premature tapetal PCD is also observed in rice anthers (Endo et al., 2009). These tapetal cells show some basic markers of apoptosis, such as membrane blebbing, fractured vacuole, structural distortion of mitochondria, and cytoplasmic degradation (Ku et al., 2003). Snider et al. (2009) reported that superoxide production and scavenging of ROS are reduced in the heat-stressed pistils of Gossypium hirsutum. Besides, heat stress induced PCD, including TUNEL-positive nuclei, cyt c release, and activation of proteases, was also reported in tomato fruit pericarp (Qu et al., 2009). Low temperature is one of the abiotic stresses as well as high temperature. It is especially important for plants growing in tropical and subtropical regions. Many of these plants are affected by the environmental temperature fall less than 10 C (Fowler et al., 2005). As reported by Ning et al. (2002), low temperature induced nuclear condensation and oligonucleosomal DNA fragmentation, which is one of the markers of PCD in maize roots. Similarly, during anther development, morphological changes, such as abnormal vacuolization, decreased division capacity, and increased peroxidase activity, are observed in rice tapetal cells exposed to chilling stress (Mamun et al., 2006).

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TABLE 1.3 Programmed cell death (PCD) related effects of high and low temperature in plants. Species

Temp. PCD-related effects

References

Nicotiana tabacum

Low

DNA condensation and fragmentation

Koukalova´ et al. (1997)

N. tabacum

High

Activation of certain oxidative stress-related genes including CSD1, Swidzinski et al. CSD3, and GPX, and activation of cysteine proteinases (2002)

N. tabacum

High

Cyt c release into cytoplasm, production of O2 2 and H2O2, activation of caspase-3-like protease

Vacca et al. (2006)

Chlorella saccharophila

High

Condensation of chromatin, DNA ladder, cell shrinkage, caspase 3 like activity

Zuppini et al. (2009)

A. thaliana

Low

Oxidative stress, activation of cysteine protease

Zhang et al. (2008)

A. thaliana

High

Apoptotic-like PCD

Doyle and McCabe (2010)

Aponogeton madagascariensis

High

Blebbing of the cell membrane, increment of vesicles containing Lord and hydrolytic enzymes, chromatin condensation, TUNEL-positive Gunawardena nuclei, increased Brownian motion within the vacuoles, decrease in (2011) ΔΨm

A. thaliana

High

KOD expression, depolarization of the mitochondrial membrane, mitochondrial dysfunction

Blanvillain et al. (2011)

Triticum aestivum

High

DNA degradation

Hameed et al. (2013)

A. thaliana

High

Upregulated transcription of cVPE, alteration of caspase-1-like activity, increased MAP kinase 6 activity

Li et al. (2012)

T. aestivum

Low

Protoplast shrinkage, DNA fragmentation, excess ROS generation, alteration in ΔΨm, and the leakage of cyt c

Lyubushkina et al. (2014)

Cucumis sativus

Low

Activations of Bax and BI-1 genes, increased electrolyte leakage, DNA fragmentation

Zhao et al. (2014)

Arabidopsis thaliana

GPX, Glutathione peroxidase; MAP, mitogen-activated protein.

1.4.2 Drought- and flooding-induced programmed cell death Drought is described as natural phenomena in which rainfalls significantly drop less than the recorded normal levels (Larcher, 1995). Drought stress is caused by a combination of water deficit, high temperature, and high solar radiation triggering decline of CO2 assimilation rates, reduction of leaf size, expansion of stems, root proliferation, alterations in plant water interactions, reduced water-use efficiency, osmolyte accumulation, generation of ROS, and increased antioxidative systems (Anjum et al., 2011). Although there are many physiological and molecular studies subjected drought stress, only a few have been reported drought-induced PCD. It has been reported that drought-induced PCD leads to

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TABLE 1.4 Programmed cell death (PCD) related effects of drought and flooding in plants. Plant species

Condition PCD-related effects

References

Pisum sativum

Flooding

Abnormalities in root tip morphology, TUNEL-positive reaction, DNA fragmentation, and cytoplasmic shrinkage

Gladish et al. (2006)

Oryza sativa

Drought

TUNEL-positive reaction, increased concentration of H2O2, and downregulation of antioxidant transcripts

Nguyen et al. (2009)

A. thaliana

Drought

Degradation of organelles, increased size of the vacuole, plasmalemma collapse, accumulation of ROS, expression of BAX inhibitor-1

Duan et al. (2010)

Triticum aestivum

Drought

DNA fragmentation, lipid peroxidation, enhanced protease, and ascorbate Hameed peroxidase activities et al. (2013)

Zea mays

Flooding

Increase in H2O2 content, DNA fragmentation, increased ethylene and polyamine concentrations, and increment of PCD-related proteins

Chen et al. (2014)

ROS, Reactive oxygen species.

ROS accumulation, DNA fragmentation, organelle degeneration, and cytoplasm shrinkage (Nguyen et al., 2009; Duan et al., 2010; Hameed et al., 2013). Microspore abortion resulting male sterility is one of the prominent problems arising during periods of drought. This situation is as a consequence to ROS increase following periods of water deficit causing microspore PCD (De Storme and Geelen, 2014). Nguyen et al. (2009) reported that short-term drought treatment resulted in the accumulation of H2O2 in rice anthers. Subsequently reduced transcription of antioxidant enzymes, ATP depletion, and DNA fragmentation were also observed. Flooding is one of the major problems affecting plant growth and development in many agricultural regions worldwide. Flooding results from heavy rainfall or overflow of water sources, and therefore a water layer on the soil surface occurs (Aggarwal et al., 2006). Long-term flooding stress results from lack of oxygen molecule initially. Accordingly, the soil oxidation potential progressively decreases (Striker, 2012). Flooding stress studies are mostly focused on the effects on plant morphology and physiology, such as adventitious root formation, increment in stem elongation, stomata closure, reduction of transpiration, inhibition of photosynthesis, ethylene production, and aerenchyma formation in the root cortex (Striker et al., 2005; Grimoldi et al., 2005; Seago et al., 2005; Pucciariello et al., 2014). Principally lysigenous aerenchyma occurs from the collapse and lysis of parenchymatic cells in the root cortical cells (Takahashi et al., 2014). It has been stated that during flooding, oxygen deficiency and ethylene accumulation trigger aerenchyma formation through PCD (Gunawardena et al., 2001; Striker, 2012). Subbaiah and Sachs (2003) reported that flooding induces rise in cytosolic Ca21, alterations of ionic homeostasis, and root tip death in maize. Lenochova´ et al. (2009) also indicated aerenchyma formation during flooding stress with the results of TUNEL-positive nuclei and ultrastructural changes in cortical cells. They suggested that ethylene triggers aerenchyma formation through PCD. Only few studies demonstrating the relation between drought/flooding induced PCD were available in higher plants (Table 1.4).

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1.4.3 Salinity-induced programmed cell death Salinity is a substantial problem limiting plant growth and productivity. It has affected more than 20% of the cultivated area in the world (Qadir et al., 2014). Salinity is a consequence of salt accumulation in the arid and semiarid climatic regions. In these regions, salts are released from the upper parts of soil by evaporation (Ekmekc¸i et al., 2005). Salt stress affects the plant cells in two ways: (1) osmotic effect by preventing water intake from soil solution and (2) ionic effect by altering physiological events. The osmotic effect causes a reduction in cell expansion and division (La¨uchli and Grattan, 2007; Munns and Tester, 2008). The salinity stress causes various alterations in plant metabolism, such as interruption of membranes, nutrient imbalance, decreased photosynthetic activity, metabolic toxicity, inhibition of K1 uptake, impairment of ROS detoxification, and cell death (Botella et al., 2005; Munns and Tester, 2008; Hong et al., 2010). Although salinity-induced PCD mechanism is still unknown, the researchers suggest that changes in the cytosolic K1/Na1 ratio may be influential for triggering PCD (Shabala et al., 2006). Salinity-induced PCD was reported by Huh et al. (2002) in yeast and plants. The researchers indicated that salt stress caused DNA fragmentation, vacuolization, cell lysis, and increment of Bcl-2 protein in yeast. They also demonstrated nuclear fragmentation by TUNEL in A. thaliana wild-type and sos1 mutant. Hallmarks of plant PCD, such as increased ROS level, DNA fragmentation, decrease mitochondrial membrane potential, and MPTP opening, were shown on Nicotiana tabacum protoplasts by Lin et al. (2006), and the authors stated that changed cellular redox state provides as a signal of the induction phase of PCD by the opening of MPTP. Salt stress induced ROS biosynthesis in vegetative and generative cells has been shown to induce PCD. The polarization of mitochondria in the seed lines of unstressed individuals and the mitochondrial depolarization in gametophytes of stressed individuals suggest that the change in ΔΨm is a signal that stimulates PCD (Hauser et al., 2006). Similarly, it was found that salt-stressed ovules of Brassica napus were blunted in most of the individuals, whereas gametophytic cells contained abundant vacuoles, and the nuclei were broken down in nonblunted ovules (Mahmoodzadeh et al., 2009). Several studies demonstrated that high salinity effectively leads to PCD in higher plants (Table 1.5).

1.4.4 Ultraviolet-induced programmed cell death According to the diverse wavelengths of electromagnetic radiation, solar radiation is grouped into three classes: (1) UV radiation (UV , 400 nm), (2) active photosynthetic radiation (photosynthetically active radiation (PAR)B400 700 nm), and (3) far-red radiation (B700 780 nm). A total of 7% 9% of the total solar radiation reaching to the earth’s surface constitutes UV radiation. It is composed of UV-C (200 280 nm) and UV-B radiation (280 320 nm). UV-C and UV-B radiations are absorbed by atmospheric gases and stratospheric ozone layer, respectively. Besides, a very small amount of UV-A radiation (320 390 nm) also reaches to the earth’s surface, but it cannot be absorbed by the ozone ´ and transmitted to the earth’s surface completely (Danon and Gallois, 1998; Wituszynska ´ and Karpinski, 2013). UV-A is less damaging than UV-B and -C. Among these, UV-B comes forward according to impacts on the plant growth and development

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1.4 Abiotic stress and programmed cell death

TABLE 1.5 Programmed cell death (PCD) related effects of salt stress in plants. Plant species

NaCI concentrations PCD-related effects

References

Nicotiana tobacum

200 mM

Increment of cytosolic Ca , decrease in ΔΨm

Lin et al. (2006)

Oryza sativa

500 mmol/L

ROS accumulation, increase of the antioxidant enzyme activity, DNA fragmentation, nuclear condensation and deformation, TUNEL-positive reaction, and cyt c release

Li et al. (2007)

O. sativa

500 mM

Decreased integrity of mitochondria, small release of cyt c, DNA fragmentation, upregulation of PCD-related proteins.

Cheng et al. (2009)

Thellungiella halophila

300 mM

Cytoplasmic shrinkage, chromatin condensation, DNA laddering, cyt c release, and activation of caspase 3 like protease activity

Wang et al. (2010)

N. tabacum

100 and 200 mM

Mitochondrial dysfunction, NADPH-oxidase-dependent O2 2 generation

Monetti et al. (2014)

Cakile maritima and A. thaliana

50, 200, and 400 mM

Oxidative stress, dysfunction of mitochondria, and caspaselike activity

Hamed-Laouti et al. (2016)

21

ROS, Reactive oxygen species.

(Hollosy et al., 2002). UV-B level increases because of anthropogenic air pollution; as a result, the ozone layer has got thinner by 5% (Caldwell et al., 2007). Low-level UV radiation activates plant defense mechanism including ROS neutralizing, repairmen of UV-induced pyrimidine dimers, and generating UV-absorbing second´ ary metabolites to protect the plant from UV damage (Kunz et al., 2006; Wituszynska ´ and Karpinski, 2013). Overexposure to UV leads to emergence PCD signals (Table 1.6) such as activation of caspase-like proteases, DNA fragmentation and damage, and apoptotic nuclear morphology in plants (Danon and Gallois, 1998; Danon et al., 2004; Gao et al., 2007).

1.4.5 Heavy metal- and nanoparticle-induced programmed cell death Heavy metals are the most common environmental pollutants affecting plant growth and productivity in the entire world. Heavy metals have a high atomic weight and a density greater than 5 g/cm3 (Adriano, 2001). Metal concentrations in the earth are originated by either as a result of human activities or geological origin of the soil, ranging from 1 to 100,000 ppm (Blaylock and Huang, 2000). Heavy metal pollution is caused by a majority of anthropogenic sources containing industrial wastes, mining, refinement, domestic effluents, vehicle emissions, coal burning, etc. (Nagajyoti et al., 2010). When the concentration of heavy metals in the soil exceeds the threshold rate, they cause toxicity on plant growth and development. The heavy metal ions react with biomolecules inducing oxidative stress due to generation of ROS (Mustafa and Komatsu, 2016). Heavy metal induced oxidative stress leads to membrane disruption, macromolecule deterioration, ion leakage, lipid peroxidation, DNA fragmentation, and cell death

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1. Abiotic stress induced programmed cell death in plants

TABLE 1.6 Programmed cell death (PCD) related effects of ultraviolet (UV) radiation in plants. Plant species

UV

PCD-related effects

References

Arabidopsis thaliana

UV-C ROS accumulation, loss of ΔΨm, and aggregated mitochondria

Gao et al. (2007)

A. thaliana

UV-C Upregulation of metacaspase 8 gene

He et al. (2008)

A. thaliana

UV-B Increased expression of radical-induced cell death 1 gene (rcd 1-1)

Jiang et al. (2009)

Nicotiana tabacum

UV-B Cell shrinkage, condensation of chromatin, micronuclei formation, DNA fragmentation, and TUNEL-positive nuclei

Lytvyn et al. (2010)

A. thaliana

UV-B Activated MAPK signaling pathway, UVR8 pathway-mediated tolerance

Gonza´lezBesteiro et al. (2011)

N. tabacum

UV-B Depolymerization of microtubule organization, shrinkage of cytoplasm, chromatin condensation, and micronuclei formation

Krasylenko et al. (2013)

A. thaliana

UV-B DNA damage, altered antioxidant metabolism, overexpressing AtPDCD5

Ferreyra et al. (2016)

MAPK, Mitogen-activated protein kinase; ROS, reactive oxygen species.

TABLE 1.7 Programmed cell death (PCD) related effects of heavy metals in plants. Plant species

Metal PCD-related effects

References

Arabidopsis thaliana

CdCl2 Increase in NO and phytochelatin synthesis, increased concentration of H2O2, expression of the marker SAG12, increased cell death

De Michele et al. (2009)

Nicotiana tabacum

CdCl2 TUNEL-positive nuclei, chromatin condensation, increasing expression of a Ma et al. PCD-related gene Hsr203J, increase in NO (2010)

Solanum nigrum

Zn

Genipa americana

CdCl2 Morphological changes in root nucleus, TUNEL-positive nuclei, and cell wall lignification

Souza et al. (2011)

Arachis hypogaea

AlCl3

DNA cleavage, chromatin condensation, apoptosis-related gene Hrs203j expression, cyt c release, caspase-3-like activity, increased the opening of MPTP, decrease in ΔΨm, and ROS production

Huang et al. (2014)

A. hypogaea

AlCl3

Caspase-1-, -2-, -3-, -4-, -5-, -6-, -8-, and -9-like proteases activity, increased root cell death, DNA fragmentation, Hrs203j expression, and TUNELpositive nuclei

Yao et al. (2016)

N. tabacum

HgCl2 Decreased cell viability, chromatin condensation and cytoplasm shrinkage, increased PCD-related gene Hrs203j expression, and TUNEL-positive nuclei

NO and ROS production, TUNEL-positive nuclei, and chromatin condensation

Xu et al. (2010)

Zi et al. (2017)

MPTP, Mitochondrial permeability transition pores; ROS, reactive oxygen species; SAG12, senescence-associated gene12.

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1.4 Abiotic stress and programmed cell death

TABLE 1.8 Programmed cell death (PCD) related effects of metal nanoparticles (NPs) heavy metals in plants. Plant species Nanoparticles PCD-related effects

References

Lycopersicon esculentum

NiO NPs

ROS increase, antioxidant enzyme activity, lipid peroxidation, increased number of apoptotic and necrotic cells, caspase-3-like activity, nuclear condensation, abundance in peroxisomes, dysfunction, and degeneration of mitochondria

Faisal et al. (2013)

Raphanus sativus

Fe2O3 NPs

Degeneration of mitochondria, vacuolization, ROS increase, reduced ΔΨm, Ca21 influx, antioxidant enzyme activity, and DNA fragmentation

Saquib et al. (2016)

Solanum melongena

Co3O4 NPs

Degeneration of mitochondria, abundance of peroxisomes, vacuolization, ROS increase, reduced ΔΨm, and DNA fragmentation

Faisal et al. (2016)

Arabidopsis thaliana

CuO NPs

ROS increase, upregulation of PCD related genes

Tang et al. (2016)

Triticum aestivum L.

Al2O3 NPs

Decreased mitotic index, chromosomal abnormalities, loss of plasma membrane integrity, irregular microtubule aggregations, TUNELpositive nuclei, and caspase-like activities

Yanık et al. (2017)

Allium cepa

Fe0—NPs

ROS increase, lipid peroxidation, electrolyte leakage, reduced ΔΨm, antioxidant enzyme activities, DNA damage, nuclear aberrations, micronuclei formation, and increased apoptotic and necrotic cells

Ghosh et al. (2017)

ROS, Reactive oxygen species.

(Chen et al., 2012). Various heavy metals were shown to induce PCD in plants (Table 1.7). In Chenopodium botrys, abnormalities in the development of heavy metal stressed ovules were detected as rapid blunting in embryonic cells and irregularities in the nuclei (Yousefı et al., 2011). A recent study indicated that mercury leaded to PCD by decreasing cell viability, chromatin condensation, and cytoplasm shrinkage and increasing Hrs203j expression and TUNEL-positive nuclei at N. tabacum (Zi et al., 2017). In addition to heavy metals, along with the advances in nanotechnology metal, NPs are widely used materials in the areas of electric and electronics, biomedical sciences, pharmaceutical industry, cosmetic products, water filtration systems, catalytic systems, manufacturing, health care, and medical diagnosis (Nowack and Bucheli, 2007). The widespread use of NPs can cause release into the environment and is expected to accumulate different compartments of the environment, such as fresh water, air, soil, and agricultural areas (Cornelis et al., 2014). NP studies on plants indicated apparent phytotoxicity with regard to morphological, physiological, and molecular symptoms (Deng et al., 2014). Some studies on NP phytotoxicity focused on morphological and anatomical parameters, such as germination index, root length, shoot/root biomass, and root morphology (Yang and Watts, 2005; Lin and Xing, 2007; Lee et al., 2008; Liu et al., 2010). Recent studies in different plant species reported that NPs cause reductions in mitotic index, damage in root cap and epidermal cells, DNA and chromosomal damage, up and downregulation of various stress-related

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1. Abiotic stress induced programmed cell death in plants

genes, antioxidant enzyme activity, lipid peroxidation, and cell death due to the formation of ROS (Rico et al., 2011; Nair and Chung, 2014; Chen et al., 2015; Nagaonkar et al., 2015; Hossain et al., 2016; Tripathi et al., 2017). Some of the studies subjected NPs-induced PCD, which were summarized in Table 1.8.

1.5 Concluding remarks and future perspectives In this chapter, we have focused the cellular events related to ROS generation and caspase-like activities during abiotic stress induced PCD. PCD is a crucial process in plant development and during environmental (biotic abiotic) stress conditions. Although morphological and biochemical mechanisms of PCD are identified, the genes, proteins, and regulatory networks involved in abiotic stress induced PCD still remain unclear in plants. Besides, during combined stress conditions (e.g., drought and salinity), plants give different responses at the molecular level. Physiological and molecular characterization of stress-induced PCD will lead in the future to a better understanding of the mechanisms of abiotic stress and tolerance in environmental and agricultural systems, which will enhance ultimately to develop high-yielding and more resident crop varieties.

References Adriano, D.C., 2001. Trace Elements in Terrestrial Environments. Springer. Aggarwal, P.K., Banerjee, B., Daryaei, M.G., Bhatia, A., Bala, A., Rani, S., et al., 2006. InfoCrop: a dynamic simulation model for the assessment of crop yields, losses due to pests, and environmental impact of agroecosystems in tropical environments. II. Performance of the model. Agr. Syst. 89, 47 67. Ahmed, F.E., Hall, A.E., DeMason, D.A., 1992. Heat injury during floral development in cowpea (Vigna unguiculata). Am. J. Bot. 79, 784 791. An, L.H., You, R.L., 2004. Studies on nuclear degeneration during programmed cell death of synergid and antipodal cells in Triticum aestivum. Sex. Plant Reprod. 17, 195 201. Anjum, S.A., Xie, X., Wang, L., Saleem, M.F., Man, C., Lei, W., 2011. Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agric. Res. 6 (9), 2026 2032. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373 399. Bar-Dror, T., Dermastia, M., Kladnik, A., Znidaric, M.T., Novak, M.P., Meir, S., et al., 2011. Programmed cell death occurs asymmetrically during abscission in tomato. Plant Cell 23 (11), 4146 4163. Bell, P.R., 1996. Megaspore abortion: a consequence of selective apoptosis? Int. J. Plant Sci. 157 (1), 1 7. Bienert, G.P., Schjoerring, J.K., Jahn, T.P., 2006. Membrane transport of hydrogen peroxide. Biochim. Biophys. Acta 1758, 994 1003. Blanvillain, R., Young, B., Cai, Y., Hecht, V., Varoquaux, F., Delorme, V., et al., 2011. The Arabidopsis peptide kiss of death is an inducer of programmed cell death. EMBO J. 30, 1173 1183. Blaylock, M.J., Huang, J.W., 2000. Phytoextraction of metals. Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. John Wiley and Sons, p. 303. Bollhoner, B., Zhang, B., Stael, S., Denance, N., Overmyer, K., Goffner, D., et al., 2013. Post mortem function of AtMC9 in xylem vessel elements. New Phytol. 200 (2), 498 510. Bostock, R.M., Pye, M.F., Roubtsova, T.V., 2014. Predisposition in plant disease: exploiting the nexus in abiotic and biotic stress perception and response. Annu. Rev. Phytopathol. 52, 517 549. Botella, M.A., Rosado, A., Bressan, R.A., Hasegawa, P.M., 2005. Plant adaptive responses to Salinity stress. In: Jenks, M.A., Hasegawa, P.M. (Eds.), Plant Abiotic Stress. John Wiley and Sons, p. 37.

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References

17

Bozhkov, P.V., Suarez, M.F., Filonova, L.H., Daniel, G., Zamyatnin, A.A., Rodriguez-Nieto, S., et al., 2005. Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis. Proc. Natl. Acad. Sci. U.S.A. 102 (40), 14463 14468. Cai, Y.M., Yu, J., Gallois, P., 2014. Endoplasmic reticulum stress-induced PCD and caspase-like activities involved. Front. Plant Sci. 5, 41. Caldwell, M.M., Ballare, C.L., Bornman, J.F., Flint, S.D., Bjorn, L.O., Teramura, A.H., et al., 2007. Terrestrial ecosystems, increased solar ultraviolet radiation and interactions with other climatic change factors. Photochem. Photobiol. Sci. 2, 29 38. Caverzan, A., Casassola, A., Brammer, S.P., 2016. Reactive Oxygen Species and Antioxidant Enzymes Involved in Plant Tolerance to Stress. InTech Publisher, pp. 463 480. Chen, F., Gao, J., Zhou, Q., 2012. Toxicity assessment of simulated urban runoff containing polycyclic musks and cadmium in Carassius auratus using oxidative stress biomarkers. Environ. Pollut. 162, 91 97. Chen, Y., Wang, X.C., Bao, H., Zhang, W., 2014. Examination of the leaf proteome during flooding stress and the induction of programmed cell death in maize. Proteome Sci. 12, 33. Chen, J., Liu, X., Wang, C., Yin, S.S., Li, X.L., Hu, W.J., et al., 2015. Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings. J. Hazard. Mater. 297, 173 182. Cheng, Y., Qi, Y., Zhu, Q., Chen, X., Wang, N., Zhao, X., et al., 2009. New changes in the plasma-membraneassociated proteome of rice roots under salt stress. Proteomics 9 (11), 3100 3114. Cheung, A.Y., 1996. The pollen tube growth pathway: its molecular and biochemical contributions and responses to pollination. Sex. Plant Reprod. 9 (6), 330 336. Chichkova, N.V., Shaw, J., Galiullina, R.A., Drury, G.E., Tuzhikov, A.I., Kim, S.H., et al., 2010. Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO J. 29 (6), 1149 1161. Choi, C.J., Berges, J.A., 2013. New types of metacaspases in phytoplankton reveal diverse origins of cell death proteases. Cell Death Dis. 4, e490. Coffeen, W.C., Wolpert, T.J., 2004. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16 (4), 857 873. Coll, N.S., Smidler, A., Puigvert, M., Popa, C., Valls, M., Dangl, J.L., 2014. The plant metacaspase AtMC1 in pathogen-triggered programmed cell death and aging: functional linkage with autophagy. Cell Death Differ. 21 (9), 1399 1408. Cornelis, G., Hund-Rinke, K., Kuhlbusch, T., Van den Brink, N., Nickel, C., 2014. Fate and bioavailability of engineered nanoparticles in soils: a review. Crit. Rev. Environ. Sci. Technol. 44 (24), 2720 2764. Danon, A., Gallois, P., 1998. UV-C radiation induces apoptotic-like changes in Arabidopsis thaliana. FEBS Lett. 437 (1 2), 131 136. Danon, A., Rotari, V.I., Gordon, A., Mailhac, N., Gallois, P., 2004. Ultraviolet-C overexposure induces programmed cell death in Arabidopsis which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and Defender against Apoptotic Death. J. Biol. Chem. 279 (1), 779 787. Davletova, S., Rizhsky, L., Liang, H.J., Zhong, S.Q., Oliver, D.J., Coutu, J., et al., 2005. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17 (1), 268 281. De Michele, R., Vurro, E., Rigo, C., Costa, A., Elviri, L., Di Valentin, M., et al., 2009. Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol. 150 (1), 217 228. De Storme, N., Geelen, D., 2014. The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant Cell Environ. 37 (1), 1 18. Dellaporta, S.L., Calderon-Urrea, A., 1994. The sex determination process in maize. Science 266 (5190), 1501 1505. Deng, Y.Q., White, D.C., Xing, B.S., 2014. Interactions between engineered nanomaterials and agricultural crops: implications for food safety. J. Zhejiang Univ.-Sci. 15 (8), 552 572. Doyle, S.M., McCabe, P.F., 2010. Type and cellular location of reactive oxygen species determine activation or suppression of programmed cell death in Arabidopsis suspension. Plant Signal Behav. 5, 467 468. Drew, M.C., He, C.J., Morgan, P.W., 2000. Programmed cell death and aerenchyma formation in roots. Trends Plant Sci. 5 (3), 123 127. Duan, Y., Zhang, W., Li, B., Wang, Y., Li, K., Sodmergen, C.H., et al., 2010. An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytol. 186 (3), 681 695. ¨ J. Agric. Faculty Ekmekc¸i, E., Apan, M., Kara, T., 2005. The effects of salinity on plant growth (in Turkish). OMU 20 (3), 118 125.

Plant Life under Changing Environment

18

1. Abiotic stress induced programmed cell death in plants

Endo, M., Tsuchiya, T., Hamada, K., Kawamura, S., Yano, K., Ohshima, M., et al., 2009. High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol. 50 (11), 1911 1922. Faisal, M., Saquib, Q., Alatar, A.A., Al-Khedhairy, A.A., Hegazy, A.K., Musarrat, J., 2013. Phytotoxic hazards of NiO-nanoparticles in tomato: a study on mechanism of cell death. J. Hazard. Mater. 250, 318 332. Faisal, M., Saquib, Q., Alatar, A.A., Al-Khedhairy, A.A., Mukhtar, A., Ansari, S.M., et al., 2016. Cobalt oxide nanoparticles aggravate DNA damage and cell death in eggplant via mitochondrial swelling and NO signaling pathway. Biol. Res. 49 (1), 20. Ferreyra, M.L.F., Casadevall, R., D’Andrea, L., AbdElgawad, H., Beemster, G.T.S., Casati, P., 2016. AtPDCD5 plays a role in programmed 12 cell death after UV-B exposure in Arabidopsis. Plant Physiol. 170 (4), 2444 2460. Fowler, S., Cook, D., Thomashow, M.F., 2005. The CBF cold-response pathway. Plant responses to high temperature. Plant Abiotic Stress. Blackwell Publishing. Fukuda, H., 2000. Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol. Biol. 44 (3), 245 253. Gadjev, I., Stone, J.M., Gechev, T.S., 2008. Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. Int. Rev. Cell Mol. Biol. 270, 87 144. Gao, C., Xing, D., Li, L., Zhang, L., 2007. Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure. Planta 227 (4), 755 767. Gechev, T.S., Van Breusegem, F., Stone, J.M., Denev, I., Laloi, C., 2006. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioassays 28 (11), 1091 1101. Ghosh, I., Mukherjee, A., Mukherjee, A., 2017. In planta genotoxicity of nZVI: influence of colloidal stability on uptake, DNA damage, oxidative stress and cell death. Mutagenesis 32 (3), 371 387. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48 (12), 909 930. Gladish, D.K., Xu, J., Niki, T., 2006. Apoptosis-like programmed cell death occurs in procambium and ground meristem of pea (Pisum sativum) root tips exposed to sudden flooding. Ann. Bot. 97 (5), 895 902. Gonza´lez-Besteiro, M.A., Bartels, S., Albert, A., Ulm, R., 2011. Arabidopsis MAP kinase phosphatase 1 and its target MAP kinases 3 and 6 antagonistically determine UV-B stress tolerance, independent of the UVR8 photoreceptor pathway. Plant J. 68, 727 737. Greenberg, J.T., 1997. Programmed cell death in plant-pathogen interactions. Annu. Rev. Plant Biol. 48 (1), 525 545. Grimoldi, A.A., Insausti, P., Vasellati, V., Striker, G.G., 2005. Constitutive and plastic root traits and their role in differential tolerance to soil flooding among coexisting species of a lowland grassland. Int. J Plant Sci. 166 (5), 805 813. Gunawardena, A.H., McCabe, P.F., 2015. Plant Programmed Cell Death. Springer. Gunawardena, A.H., Pearce, D.M., Jackson, M.B., Hawes, C.R., Evans, D.E., 2001. Characterization of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212 (2), 205 214. Gunawardena, A.H., Greenwood, J.S., Dengler, N.G., 2007. Programmed cell death remodels lace plant leaf shape during development. Plant Cell 16 (1), 60 73. Hameed, A., Goher, M., Iqbal, N., 2013. Drought induced programmed cell death and associated changes in antioxidants, proteases, and lipid peroxidation in wheat leaves. Biol. Plant. 57 (2), 370 374. Hamed-Laouti, I.B., Arbelet-Bonnin, D., De Bont, L., Biligui, B., Gakie`re, B., Abdelly, C., et al., 2016. Comparison of NaCl-induced programmed cell death in the obligate halophyte Cakile maritima and the glycophyte Arabidospis thaliana. Plant Sci. 247, 49 59. Hara-Nishimura, I., Hatsugai, N., Nakaune, S., Kuroyanagi, M., Nishimura, M., 2005. Vacuolar processing enzyme: an executioner of plant cell death. Curr. Opin. Plant Biol. 8 (4), 404 408. Hasanuzzaman, M., Nahar, K., Fujita, M., 2013. Extreme temperatures, oxidative stress and antioxidant defense in plants. Abiotic Stress—Plant Responses and Applications in Agriculture. InTech, pp. 169 205. Hatfield, J.L., Prueger, J.H., 2015. Temperature extremes: effect on plant growth and development. Weather Clim. Extrem. 10, 4 10.

Plant Life under Changing Environment

References

19

Hatsugai, N., Kuroyanagi, M., Yamada, K., Meshi, T., Tsuda, S., Kondo, M., et al., 2004. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305, 855 858. Hatsugai, N., Iwasaki, S., Tamura, K., Kondo, M., Fuji, K., Ogasawara, K., et al., 2009. A novel membrane fusionmediated plant immunity against bacterial pathogens. Genes Dev. 23, 2496 2506. Hauser, B.A., Sun, K., Oppenheimer, D.G., Sage, T.L., 2006. Changes in mitochondrial membrane potential and accumulation of reactive oxygen species precede ultrastructural changes during ovule abortion. Planta 223 (3), 492 499. He, R., Drury, G.E., Rotari, V.I., Gordon, A., Willer, M., Farzaneh, T., et al., 2008. Metacaspase-8 modulates programmed cell death induced by ultraviolet light and H2O2 in Arabidopsis. J. Biol. Chem. 283 (2), 774 783. Hollosy, F., Seprodi, J., Orfi, L., Eros, D., Keri, G., Idei, M., 2002. Evaluation of lipophilicity and antitumour activity of parallel carboxamide libraries. J. Chromatogr. B780 (2), 355 363. Hong, Y., Zhang, W., Wang, X., 2010. Phospholipase D and phosphatidic acid signaling in plant response to drought and salinity. Plant Cell Environ. 33, 627 635. Hossain, Z., Mustafa, G., Sakata, K., Komatsu, S., 2016. Insights into the proteomic response of soybean towards Al2O3, ZnO, and Ag nanoparticles stress. J. Hazard Mater. 304, 291 305. Huang, W.J., Oo, T.L., He, H.Y., Wang, A.Q., Zhan, J., Li, C.Z., et al., 2014. Aluminum induces rapidly mitochondria-dependent programmed cell death in Al-sensitive peanut root tips. Bot. Stud. 55 (1), 67. Huh, G., Damsz, B., Matsumoto, T.K., Reddy, M.P., Rus, A.M., Ibeas, J.I., et al., 2002. Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J. 29, 649 659. Huysmans, M., Lema, S.A., Coll, N.S., Nowack, M.K., 2017. Dying two deaths - programmed cell death regulation in development and disease. Curr. Opin. Plant Biol. 35, 37 44. Intergovernmental Panel on Climate Change (IPCC), 2007. Climate change 2007: Synthesis report. In: Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva, Switzerland, pp. 104. Jiang, L., Wang, Y., Bjo¨rn, L.O., Li, S., 2009. Arabidopsis radical-induced cell death1 is involved in UV-B. Photochem. Photobiol. Sci. 8, 838 846. Kacprzyk, J., Daly, C.T., Mccabe, P.F., 2011. The botanical dance of death: programmed cell death in plants. Advances in Botanical Research. Elsevier, pp. 169 261. Kisselev, A.F., Garcia-Calvo, M., Overkleeft, H.S., Peterson, E., Pennington, M.W., Ploegh, H.L., et al., 2003. The caspase-like sites of proteasomes, their substrate specificity, new inhibitors and substrates, and allosteric interactions with the trypsin-like sites. J. Biol. Chem. 278 (38), 35869 35877. Koukalova´, B., Kovaˇr´ık, A., Fajkus, J., Siroky´, J., 1997. Chromatin fragmentation associated with apoptotic changes in tobacco cells exposed to cold stress. FEBS Lett. 414 (2), 289 292. Krasylenko, Y.A., Yemets, A.I., Blume, Y.B., 2013. Plant microtubules reorganization under the indirect UV-B exposure and during UV-B-induced programmed cell death. Plant Signal. Behav. 8 (5), e24031. Ku, S., Yoon, H., Suh, H.S., Chung, Y.Y., 2003. Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta 217 (4), 559 565. Kunz, B.A., Cahill, D.M., Mohr, P.G., Osmond, M.J., Vonarx, E.J., 2006. Plant responses to UV radiation and links to pathogen resistance. Int. Rev. Cytol. 255, 1 40. Kuriyama, H., Fukuda, H., 2002. Developmental programmed cell death in plants. Curr. Opin. Plant Biol. 5 (6), 568 573. Kuroyanagi, M., Nishimura, M., Hara-Nishimura, I., 2002. Activation of Arabidopsis vacuolar processing enzyme by self-catalytic removal of an auto-inhibitory domain of the C-terminal propeptide. Plant Cell Physiol. 43 (2), 143 151. Kwak, J.M., Nguyen, V., Schroeder, J.I., 2006. The role of reactive oxygen species in hormonal responses. Plant Physiol. 141 (2), 323 329. Lam, E., 2004. Controlled cell death, plant survival and development. Nat. Rev. Mol. Cell Biol. 5 (4), 305 315. Larcher, W., 1995. Physiological Plant Ecology. Springer. Larkindale, J., Mishkind, M., Vierling, E., 2005. Plant responses to high temperature. Plant Abiotic Stress. Blackwell Publishing. La¨uchli, A., Grattan, S.R., 2007. Plant growth and development under salinity stress. Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops. Springer, pp. 1 32.

Plant Life under Changing Environment

20

1. Abiotic stress induced programmed cell death in plants

Lee, W.M., An, Y.J., Yoon, H., Kweon, H.S., 2008. Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environ. Toxicol. Chem. 27 (9), 1915 1921. Lenochova´, Z., Soukup, A., Votrubova´, O., 2009. Aerenchyma formation in maize roots. Biol. Plant. 53 (2), 263 270. Li, D.H., Yang, X., Cui, M.K., 2003. Morphological changes in nucellar cells undergoing programmed cell death (PCD) during pollen chamber formation in Ginkgo biloba. Acta Bot. Sin. 45 (1), 53 63. Li, J., Jiang, A., Chen, H., Wang, Y., Zhang, W., 2007. Lanthanum prevents salt stress-induced programmed cell death in rice root tip cells by controlling early induction events. J. Integr. Plant Biol. 49, 1024 1031. Li, Z., Yue, H., Xing, D., 2012. MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytol. 195, 85 96. Lim, P.O., Kim, H.J., Nam, H.G., 2007. Leaf senescence. Annu. Rev. Plant Biol. 58, 115 136. Lin, D., Xing, B., 2007. Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ. Pollut. 150 (2), 243 250. Lin, J., Wang, Y., Wang, G., 2006. Salt stress-induced programmed cell death via Ca21-mediated mitochondrial permeability transition in tobacco protoplasts. Plant Growth Reg. 45, 243 250. Liu, Q., Zhao, Y., Wan, Y., Zheng, J., Zhang, X., Wang, C., et al., 2010. Study of the inhibitory effect of watersoluble fullerenes on plant growth at the cellular level. ACS Nano 4 (10), 5743 5748. Lord, C.E., Gunawardena, A.H., 2011. Environmentally induced programmed cell death in leaf protoplasts of Aponogeton madagascariensis. Planta 233 (2), 407 421. Lord, C.E., Gunawardena, A.H., 2012. Programmed cell death in C. elegans, mammals and plants. Eur. J. Cell Biol. 91 (8), 603 613. Lytvyn, D.I., Yemets, A.I., Blume, Y.B., 2010. UV-B overexposure induces programmed cell death in a BY-2 tobacco cell line. Environ. Exp. Bot. 68 (1), 51 57. Lyubushkina, I.V., Grabelnych, O.I., Pobezhimova, T.P., Stepanov, A.V., Fedyaeva, A.V., Fedoseeva, I.V., et al., 2014. Winter wheat cells subjected to freezing temperature undergo death process with features of programmed cell death. Protoplasma 251, 615 623. Ma, W., Xu, W., Xu, H., Chen, Y., He, Z., Ma, M., 2010. Nitric oxide modulates cadmium influx during cadmiuminduced programmed cell death in tobacco BY-2 cells. Planta 232 (2), 325 335. Madlung, A., Comai, L., 2004. The effect of stress on genome regulation and structure. Ann. Bot. 94 (4), 481 495. Mahmoodzadeh, H., Kabiri, M., Branch, M., 2009. A normal micro-and megagametophyte development in Brassica napus induced by high salinity. Res. J. Environ. Sci. 3 (5), 514 521. Mamun, E.A., Alfred, S., Cantrill, L.C., Overall, R.L., Sutton, B.G., 2006. Effects of chilling on male gametophyte development in rice. Cell Biol. Int. 30 (7), 583 591. McStay, G.P., Salvesen, G.S., Green, D.R., 2007. Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death Differ. 15 (2), 322 331. Misas-Villamil, J.C., Toenges, G., Kolodziejek, I., Sadaghiani, A.M., Kaschani, F., Colby, T., et al., 2013. Activity profiling of vacuolar processing enzymes reveals a role for VPE during oomycete infection. Plant J. 73 (4), 689 700. Mishra, N.S., Tuteja, R., Tuteja, N., 2006. Signaling through MAP kinase networks in plants. Arch. Biochem. Biophys. 452 (1), 55 68. Monetti, E., Kadono, T., Tran, D., Azzarello, E., Arbelet-bonnin, D., Biligui, B., et al., 2014. Deciphering early events involved in hyperosmotic stress-induced programmed cell death in tobacco BY-2 cells. J. Exp. Bot. 65, 1361 1375. Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Ann. Rev. Plant Biol. 59, 651 681. Mustafa, G., Komatsu, S., 2016. Toxicity of heavy metals and metal-containing nanoparticles on plants. Biochim. Biophys. Acta 1864 (8), 932 944. Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8 (3), 199 216. Nagaonkar, D., Shende, S., Rai, M., 2015. Biosynthesis of copper nanoparticles and its effect on actively dividing cells of mitosis in Allium cepa. Biotechnol. Prog. 31 (2), 557 565. Nair, P.M.G., Chung, I.M., 2014. Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignification and molecular level changes. Environ. Sci. Pollut. Res. 21 (22), 12709 12722. Nath, K., Lu, Y., 2015. A paradigm of reactive oxygen species and programmed cell death in plants. J. Cell Sci. Ther. 6 (2), 1 2.

Plant Life under Changing Environment

References

21

Nguyen, G.N., Hailstones, D.L., Wilkes, M., Sutton, B.G., 2009. Drought-induced oxidative conditions in rice anthers leading to a programmed cell death and pollen abortion. J. Agron. Crop Sci. 195 (3), 157 164. Ning, S.B., Song, Y.C., Damme, P.V., 2002. Characterization of the early stages of programmed cell death in maize root cells by using comet assay and the combination of cell electrophoresis with annexin binding. Electrophoresis 23 (13), 2096 2102. Nowack, B., Bucheli, T.D., 2007. Occurrence, behavior and effects of nanoparticles in the environment. Environ. Pollut. 150 (1), 5 22. Olvera-Carrillo, Y., van Bel, M., van Hautegem, T., Fendrych, M., Huysmans, M., Simaskova, M., et al., 2015. A conserved core of programmed cell death indicator genes discriminates developmentally and environmentally induced programmed cell death in plants. Plant Physiol. 169 (4), 2684 2699. Ott, M., Gogvadze, V., Orrenius, S., Zhivotovsky, B., 2007. Mitochondria, oxidative stress, and cell death. Apoptosis 12 (5), 913 922. Papini, A., Tani, G., Di Falco, P., Brighigna, L., 2010. The ultrastructure of the development of Tillandsia (Bromeliaceae) trichome. Flora 205 (2), 94 100. Petrov, V., Hille, J., Mueller-Roeber, B., Gechev, T.S., 2015. ROS-mediated abiotic stress-induced programmed cell death in plants. Front. Plant Sci. 6 (69). Pitzschke, A., Hirt, H., 2009. Disentangling the complexity of mitogen-activated protein kinases and reactive oxygen species signaling. Plant Physiol. 149 (2), 606 615. Pitzschke, A., Forzani, C., Hirt, H., 2006. Reactive oxygen species signaling in plants. Antioxid. Redox Signal. 8 (9 10), 1757 1764. Pucciariello, C., Voesenek, L.A., Perata, P., Sasidharan, R., 2014. Plant responses to flooding. Front. Plant Sci. 5 (226), 1 2. Qadir, M., Quillerou, E., Nangia, V., Murtaza, G., Singh, M., Thomas, R.J., et al., 2014. Economics of salt-induced land degradation and restoration. Nat. Res. Forum 38 (4), 282 295. Qi, Y., Wang, H., Zou, Y., Liu, C., Liu, Y., Wang, Y., et al., 2010. Over-expression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Lett. 585 (1), 231 239. Qu, G.Q., Liu, X., Zhang, Y.L., Yao, D., Ma, Q.M., Yang, M.Y., et al., 2009. Evidence for programmed cell death and activation of specific caspase-like enzymes in the tomato fruit heat stress response. Planta 229 (6), 1269 1279. Rantong, G., Gunawardena, A.H., 2015. Programmed cell death: genes involved in signaling regulation, and execution in plants and animals. Botany 93 (4), 193 210. Rautengarten, C., Steinhauser, D., Bu¨ssis, D., Stintzi, A., Schaller, A., Kopka, J., et al., 2005. Inferring hypotheses on functional relationships of genes: analysis of the Arabidopsis thaliana subtilase gene family. PLoS Comput. Biol. 1 (4), e40. Reape, T.J., McCabe, P.F., 2008. Apoptotic-like programmed cell death in plants. New Phytol. 180 (1), 13 26. Reape, T.J., Brogan, N.P., McCabe, P.F., 2015. Mitochondrion and chloroplast regulation of plant programmed cell death. Plant Programmed Cell Death. Springer, pp. 33 54. Rico, C.M., Majumdar, S., Duarte-Gardea, M., 2011. Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric. Food Chem. 59 (8), 3485 3498. Rocha, G.L., Fernandez, J.H., Oliveira, A.E.A., Fernandes, K.V.S., 2017. Programmed Cell Death-Related Proteases in Plants. In Tech. Rodriguez, M.C., Petersen, M., Mundy, J., 2010. Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61, 621 649. Rotari, V.I., Dando, P.M., Barret, A.J., 2001. Legumain forms from plants and animals differ in their specificity. Biol. Chem. 382 (6), 953 959. Salvesen, G.S., Hempel, A., Coll, N.S., 2016. Protease signaling in animal and plant-regulated cell death. FEBS J. 283 (14), 2577 2598. Saquib, Q., Faisal, M., Alatar, A.A., Al-Khedhairy, A.A., Ahmed, M., Ansari, S.M., et al., 2016. Genotoxicity of ferric oxide nanoparticles in Raphanus sativus: deciphering the role of signaling factors, oxidative stress and cell death. J. Environ. Sci. 47, 49 62. Seago, J.L., Marsh, L.C., Stevens, K.J., Soukup, A., Vortubova´, O., Enstone, D.E., 2005. A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Ann. Bot. 96 (4), 565 579.

Plant Life under Changing Environment

22

1. Abiotic stress induced programmed cell death in plants

Sexton, K.B., Witte, M.D., Blum, G., Bogyo, M., 2007. Design of cell-permeable fluorescent activity-based probes for the lysosomal cysteine protease asparaginylendopeptidase (AEP)/legumain. Bioorg. Med. Chem. Lett. 17 (3), 649 653. Shabala, S., Demidchik, V., Shabala, L., Cuin, T.A., Smith, S.J., Miller, A.J., et al., 2006. Extracellular Ca21 ameliorates NaCl-induced K1 loss from Arabidopsis root and leaf cells by controlling plasma membrane K1-permeable channels. Plant Physiol. 141, 1653 1665. Sharma, P., Jha, A.B., Dubey, R.S., Pessarakli, M., 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. 2012, 217037. Shiu, S.H., Bleecker, A.B., 2001. Plant receptor-like kinase gene family: diversity, function and signaling. Sci. Stke. 113 (113). Shiu, S.H., Bleecker, A.B., 2003. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132 (2), 530 543. Shiu, S.H., Karlowski, W.M., Pan, R., Tzeng, Y., Mayer, K.F.X., Li, W., 2004. Comparative analysis of the receptorlike kinase family in Arabidopsis and rice. Plant Cell 16 (5), 1220 1234. Sinha, A.K., Jaggi, M., Raghuram, B., Tuteja, N., 2011. Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal. Behav. 6 (2), 196 203. Snider, J.L., Oosterhuis, D.M., Skulman, B.W., Kawakami, E.M., 2009. Heat stress-induced limitations to reproductive success in Gossypium hirsutum. Physiol. Plant 137 (2), 125 138. Son, Y., Cheong, Y.K., Kim, N.H., Chung, H.T., Kang, D.G., Pae, H.O., 2011. Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways? J. Signal Trans. 2011, 792639. Souza, V.L., de Almedia, A.A.F., Lima, S.T.G., Cascardo, J.C.M., Silva, D.C., Mangabeira, P.A.O., et al., 2011. Morphophysiological responses and programmed cell death induced by cadmium in Genipa americana L. (Rubiaceae). Biometals 24 (1), 59 71. Striker, G.G., 2012. Flooding Stress on Plants: Anatomical, Morphological and Physiological Responses. Striker, G.G., Insausti, P., Grimoldi, A.A., Ploschuk, E.L., Vasellati, V., 2005. Physiological and anatomical basis of differential tolerance to soil flooding of Lotus corniculatus L. and Lotus glaber Mill. Plant Soil 276 (1), 301 311. Subbaiah, C.C., Sachs, M.M., 2003. Molecular and cellular adaptations of maize to flooding stress. Ann. Bot. 91 (2), 119 127. Sung, D.Y., Kaplan, F., Lee, K.J., Guy, C.L., 2003. Acquired tolerance to temperature extremes. Trends Plant Sci. 8 (4), 179 187. Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G., 2012. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35 (2), 259 270. Swidzinski, J.A., Sweetlove, L.J., Leaver, C.J., 2002. A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J. 30, 431 446. Takahashi, H., Yamauchi, T., Colmer, T.D., et al., 2014. Aerenchyma formation in plants. Low-Oxygen Stress in Plants. Springer, pp. 247 265. Tang, Y., He, R., Zhao, J., Nie, G., Xu, L., Xing, B., 2016. Oxidative stress-induced toxicity of CuO nanoparticles and related toxicogenomic responses in Arabidopsis thaliana. Environ. Pollut. 212, 605 614. Tripathi, L.P., Sowdhamini, R., 2006. Cross genome comparisons of serine proteases in Arabidopsis and rice. BMC Genomics 7 (1), 200. Tripathi, D.K., Gaur, S., Singh, S., Singh, S., Pandey, R., Singh, V.P., et al., 2017. An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiol. Biochem. 110, 2 12. Tsiatsiani, L., Van Breusegem, F., Gallois, P., Zavialov, A., Lam, E., Bozhkovhkov, P.V., 2011. Metacaspases. Cell Death Differ. 18 (8), 1279 1288. Tuzhikov, A.I., Vartapetian, B.B., Vartapetian, A.B., Chichkova, N.V., 2011. Abiotic stress-induced programmed cell death in plants: a phytaspase connection. Abiotic Stress Response in Plants-Physiological, Biochemical and Genetic Perspectives. InTech. Uren, A.G., O’Rourke, K., Aravind, L., Pisabarro, M.T., Seshagiri, S., Koonin, E.V., et al., 2000. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6 (2000), 961 967.

Plant Life under Changing Environment

References

23

Vacca, R.A., Valenti, D., Bobba, A., Merafina, R.S., Passarella, S., Marra, E., 2006. Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco BrightYellow 2 cells en route to heat shock-induced cell death. Plant Physiol. 141 (1), 208 219. van Doorn, W.G., Woltering, E.J., 2005. Many ways to exit? Cell death categories in plants. Trends Plant Sci. 10 (3), 117 122. ¨ nal, M., 2008. Proteolytic Enzymes in plant programmed cell death. Tu¨rk Bilimsel Derlemeler Dergisi Vardar, F., U 1 (1), 65 78. ¨ nal, M., 2011. Anther development and cytochemistry in Lathyrus undulatus Boiss. (Fabaceae). Acta Vardar, F., U Bot. Croat. 70, 53 64. ¨ nal, M., 2012. Ultrastructural aspects and programmed cell death in the tapetal cells of Lathyrus unduVardar, F., U latus Boiss. Acta Biol. Hung. 63 (1), 52 66. ¨ ., Aydın, Y., 2016. Determination of aluminum induced programmed cell death Vardar, F., C ¸ abuk, E., Aytu¨rk, O characterized by DNA fragmentation in Gramineae species. Caryologia 69 (2), 111 115. Vartapetian, A.B., Tuzhikov, A.I., Chichkova, N.V., Taliansky, M., Wolpert, T.J., 2011. A plant alternative to animal caspases: subtilisin-like proteases. Cell Death Differ. 18 (8), 1289 1297. Vercammen, D., van de Cotte, B., de Jaeger, G., Eeckhout, D., Casteels, P., Vandepoele, K., et al., 2004. Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J. Biol. Chem. 279 (44), 45329 45336. Wang, H., Li, J., Bostock, R.M., Gilchrist, D.G., 1996a. Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8 (3), 375 391. Wang, M., Oppedijk, B.J., Lu, X., Van Duijn, V., Schilperoort, R.A., 1996b. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol. Biol. 32 (6), 1125 1134. Wang, J., Li, X., Liu, Y., Zhao, X., 2010. Salt stress induces programmed cell death in Thellungiella halophile suspension-cultured cells. J. Plant Physiol. 167 (14), 1145 1151. Watanabe, N., Lam, E., 2005. Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J. Biol. Chem. 280 (15), 14691 14699. Wei, C.X., Lan, S.Y., Xu, Z.X., 2002. Ultrastructural features of nucleus degradation during programmed cell death of starchy endosperm cells in rice. Acta Bot. Sin. 44 (12), 1396 1402. Williams, B., Verchot, J., Dickman, M.B., 2014. When supply does not meet demand-ER stress and plant programmed cell death. Front. Plant Sci. 5, 211. ´ ´ Wituszynska, W., Karpinski, S., 2013. Programmed cell death as a response to high light, UV and drought stress in plants. Abiotic Stress Plant Responses and Applications in Agriculture. InTech, pp. 207 246. Woffenden, B.J., Freeman, T.B., Beers, E.P., 1998. Proteasome inhibitors prevent tracheary element differentiation in Zinnia mesophyll cell cultures. Plant Physiol. 118, 419 430. Woltering, E.J., 2004. Death proteases come alive. Trends Plant Sci. 9 (10), 469 472. Woo, H.R., Kim, H.J., Nam, H.G., Lim, P.O., 2013. Plant leaf senescence and death regulation by multiple layers of control and implications for aging in general. J. Cell Sci. 126 (121), 4823 4833. Wredle, U., Walles, B., Hakman, I., 2001. DNA fragmentation and nuclear degradation during programmed cell death in the suspensor and endosperm of Vicia faba. Int. J. Plant Sci. 162 (5), 1053 1063. Xu, J., Yin, H., Li, Y., Liu, X., 2010. Nitric oxide ıs associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol. 154 (3), 1319 1334. Yang, L., Watts, D.J., 2005. Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicol. Lett. 158 (2), 122 132. ¨ ., Vardar, F., 2017. Programmed cell death evidence in wheat (Triticum aestivum L.) roots Yanık, F., Aytu¨rk, O induced by aluminum oxide (Al2O3) nanoparticles. Caryologia 70, 112 119. Yao, S., Huang, W., Pan, C., Zhan, J., He, L.F., 2016. Caspase-like proteases regulate aluminum-induced programmed cell death in peanut. Plant Cell Tiss. Organ Cult. 127 (3), 691 703. Yousefı, N., Chehreganı, A., Malayerı, B., Lorestanı, B., Cheraghı, M., 2011. Investigating the effect of heavy metals on developmental stages of anther and pollen in Chenopodium botrys L. (Chenopodiaceae). Biol. Trace Elem. Res. 140, 368 376. Zaninotto, F., Camera, S.L., Polverari, A., Delledonne, M., 2006. Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol. 141 (2), 379 383.

Plant Life under Changing Environment

24

1. Abiotic stress induced programmed cell death in plants

Zhang, X., Liu, S., Takano, T., 2008. Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol. Biol. 68, 131 143. Zhao, Y., Chen, J., Tao, X., Zheng, X., Mao, L., 2014. The possible role of BAX and BI-1 genes in chilling-induced cell death in cucumber fruit. Acta Physiol. Plant 36, 1345 1351. Zi, L., Jiang, L.P., Liu, X.F., Zhong, L.F., Xue, X.X., 2017. Influence of boron deprivation on Hg stress-induced programmed cell death in suspension-cultured tobacco BY-2 cells. J. Plant Nutr. 40 (16), 2336 2348. Zuppini, A., Gerotto, C., Moscatiello, R., Bergantino, E., Baldan, B., 2009. Chlorella saccharophila cytochrome f and its involvement in the heat shock response. J. Exp. Bot. 60, 4189 4200.

Plant Life under Changing Environment

C H A P T E R

2 Regulation of temperature stress in plants Sanjesh Tiwari1, Anuradha Patel1, Madhulika Singh2 and Sheo Mohan Prasad1 1

Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India 2Centre of Advance Studies, Department of Botany, Banaras Hindu University, Varanasi, India

2.1 Introduction Plant, during its entire life cycle, from seedling to reproductive stage, faces changing environment that is sometimes unfavorable for its growth and developmental processes, and plants develop specific mechanism to overcome these environmental stresses. Adverse environmental factors are categorized majorly in two categories. First one is biotic factors that include pathogen and herbivore attacks, and second is abiotic factors that include drought, heat, cold, nutrient deficiency, and heavy-metal accumulation in the soil. Among these, salt, drought, and temperature affect the geographical distribution of plant species and disrupt the plant metabolism (Bolton, 2009). As a consequence, they limit the quality and quantity of food production in agriculture, reducing the food supply for growing population (Fedoroff et al., 2010), and to overcome these adverse effects tolerance mechanism in plants have been well studied (Abuqamar et al., 2009; Mengiste et al., 2003; Suzuki et al., 2005). In general, various environmental factors (biotic and abiotic) induce the plant resistance by activation of stress tolerance genes. The average temperature was found to be increased by 0.2
C/year and it has to be increased by 1.8
C4
C at the end of year 2100, hence temperature is pondered to be one of the utmost detrimental stress (Hasanuzzaman et al., 2013). Climate change due to temperature is a global concern that has altered the physiological and biochemical activities of plant, thereby reducing the productivity of crops (Hasanuzzaman et al., 2012, 2013). Increased temperature continuously caused heat stress in plants, which depends upon the quality, intensity, and duration of light. Generation of reactive oxygen species (ROS) is a common phenomenon exhibited by

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00002-3

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© 2020 Elsevier Inc. All rights reserved.

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2. Regulation of temperature stress in plants

all environmental factors (biotic and abiotic), including heat stress that damaged the macromolecules, such as DNA, proteins, and lipids (Singh et al., 2016), and plants are under oxidative stress. Furthermore, heat stress also altered the expression of genes that participate in the formation of responsible for the production of osmoprotectants, detoxifying enzymes, transporters, and regulatory proteins (Semenov, 2009; Krasensky and Jonak, 2012). On contrary to this, heat stress inhibits the protein folding, affects the membrane (lipid bilayer) fluidity and cytoskeleton arrangement, and also affects the vegetative and reproductive tissue (Ruelland et al., 2009; Zinn et al., 2010). Rise in temperature up to a certain limit is beneficial for plant, which regulates the circadian rhythms in plants, regulates plant movements (opening/closing of corolla) (Van Doorn and Van Meeteren, 2003; Thines and Harmon, 2010), and also affects the geographical distribution of plants in nature. Plants susceptibility toward pathogen was also enhanced by high temperature. Infection capacity of tobacco mosaic and tomato-spotted wilt viruses was found to be increased when ambient temperature increased and cause viral diseases in tobacco (Nicotiana tabacum) and pepper (Capsicum annuum), respectively (Kira´ly et al., 2008; Moury et al., 1998). In wheat genotypes, its sensitivity toward Cochliobolus sativus (caused spot blotch) was increased associated with increase in nighttime temperature (Sharma et al., 2007). Besides heat stress, decline in ambient temperature caused chilling stress in plants, which has considerable impact on cell physiology. According to Ruelland et al. (2009), chilling causes death of cells by inhibiting enzymatic activities, rigidification of biological membranes, stabilization of the nucleic acids, generation of ROS, and impaired in photosynthesis. Low temperature induces flowering in plants known as vernalization (Kim et al., 2009) and upregulates the metabolic processes that confer the tolerance strategy of plants known as cold-hardening process (Thomashow, 1999) that leads to the accumulation of compatible solutes (sugar), membrane composition changes, and enhanced the synthesis of dehydrin-like proteins (Korn et al., 2010). Under temperature stress (heat or cold stress), plants exhibited long- and short-term responses. Long-term effects caused morphological and phenological adaptations, while short-term effects include changing in leaf orientation, more transpiration, or change the composition of membrane lipids. Heat stress induces the reduced water loss by closing the stomata, increased stomatal densities including larger xylem vessels (Srivastava et al., 2012), and plants can survive under these adverse environmental factors. Generation of ROS is an unavoidable phenomenon of aerobic, and its toxicity depends upon its concentration. At low level, it acts as signaling molecule, while at higher level, it becomes toxic and leads cell death (Baxter et al., 2014). ROS, 1 such as H2O2, O2 2 , and O2, are generated under various stress conditions, including heat stress (Suzuki et al., 2012). To cope up with damaging effects caused by ROS, every plant has an array of antioxidant systems that mitigate the adverse effects. Antioxidant system includes the following enzymatic antioxidants: superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and glutathione S-transferase (GST) and nonenzymatic antioxidants, such as cysteine, proline, nonprotein thiols, and synthesis of molecular chaperones, known as heat-shock proteins (HSPs) (Guy et al., 2008; Wahid et al., 2007; Gill and Tuteja, 2010). HSPs are major proteins extensively induced by heat stress and target the HSresponsive transcription factors that regulate the protein quality by renaturing of proteins (Qu et al., 2013). In this chapter, we briefly label the effects of low and high temperature on various physiological and biochemical constituents of plants and also alteration at molecular level seen in plants, in response to high-temperature stress. This chapter also Plant Life under Changing Environment

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2.2 Effect of temperature stress on plants

emphasizes the tolerance strategy of plants and their underlying mechanisms for transduction of HT stress signals and confers the temperature tolerance in plants.

2.2 Effect of temperature stress on plants Temperature hassle is generally demarcated as the intensification in the temperature beyond a verge level, which causes irrevocable damages to plant growth and development. Elevated temperature usually above 30
C considered being heat stress; it is a complicated function encompassing the duration of exposure, intensity, and frequency of rise in temperature (Fig. 2.1).

2.2.1 High temperature Among ever-changing environmental stresses, high temperature or heat stress is the most detrimental stress that limits the growth, various physiological and metabolic processes, and productivity of plants. Plants are sessile organisms that can’t move to the favorable environmental condition, thus are susceptible to be affected by environmental

Low-temperature stress

High-temperature stress Reduced yield and fruit weight

Changes in membrane structure

Increased oxidative stress

Protoplasmic streaming and electrolyte leakage

Reduced plant growth and death

Reduced leaf size and decrease chlorophyll content

Surface lesions on leaves and fruits

Decrease in photosynthetic rate

Abnormal curling, lobbing, and crinking of leaves

Reduced activity of antioxidants

Internal discoloration (vascular browing)

Sterility in plants formation of abnormal seed Scorching of leaves and stems, leaf abscission and senescence

Loss of vigor

FIGURE 2.1 Effect of low and high-temperature stress in plants.

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2. Regulation of temperature stress in plants

condition (Lobell and Asner, 2003). Heat stress severely affects the plant processes at all the phases, that is, from germination to growth, development, reproduction, and yield (Hasanuzzaman et al., 2013). Heat stress marks the constancy of various structural and membrane proteins, cytoskeleton structures, and RNA species and alters the efficacy of enzymes that are responsible for catalyzing enzymatic reaction (Suzuki et al., 2012). During plant growth and development, first of all processes affected by heat stress is germination (Table 2.1), showing various crops affected by heat stress. Temperature together with soil moisture significantly deteriorates the seeds and regulates the period of dormancy and differs in dry and moist seeds (Liu et al., 2017). Reduced rate of germination, delayed plant emergence, abnormal growth of seedlings, and reduced growth of radicle and plemule are chief bearings triggered by heat stress (Kumar et al., 2011). Enhanced ambient temperature also leads to loss of water content from inside cell, which shrinks the cell size and eventually inhibits the growth, and at extreme condition, plants show programed cell death due to denaturation of proteins; heat stress for a longer period causes gradual death; this damages cause leaves to shed and development of abortive flowers and fruit (Rodrı´guez et al., 2005). High temperature poses more impact on the photosynthetic efficacy of plants especially, and C3 plants are known to be majorly affected (Yang et al., 2006). Highly susceptible sites majorly affected by heat stress are altered structure of thylakoid membrane, loss and swelling of grana, and the stroma, in which carbon metabolism is carried out (Wang et al., 2009). Reduction in photosynthetic efficiency is due to the reduction of soluble proteins, that is, Rubisco binding proteins (Sumesh et al., 2008). High-temperature stress moderates the activity of various enzymes, such as sucrose phosphate synthase, adenosine diphosphate (ADP)-glucose pyrophosphorylase, and invertase, which ultimately inhibits the synthesis of starch and sucrose (Djanaguiraman et al., 2009). Heat stress reduces the leaf area, water potential, and leaf senescence; this leads to the reduction in the photosynthetic performance of photosynthesis (Greer and Weedon, 2012) and cellular damages. Heat stress negatively affects the plant reproductive system as a resultant, it causes reduced anther, reduced number of pollen, pollen viability, anther dehiscence, reduced fertilization efficiency, and formation of sterile seed and fruit (Ahamed et al., 2010). Heat stress leads to excessive production of ethylene (ET), which promotes male sterility in plants, and also constrains the important enzymes that are involved in starch metabolism, further which deteriorates the grain filling pattern of plants limiting the rate of grain filling and ultimately produces sterile grain. This stress also affects the plant in flowering stage, which results in abscission and formation of abortive flower, lowering of seed germination, and formation of less number of seed (Tan et al., 2011).

2.2.2 Low temperature Chilling or low-temperature stress also affects the several physiological and biochemical processes in plants; it alters the cellular cytoskeletal structure and its function, also depreciates the nucleic acid synthesis, protein synthesis, imbalances the water and nutrient cycle, and inhibits the photosynthetic and respiratory metabolisms. Chilling injury has been categorized into two groups on the basis of direct and indirect effects, which are

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2.2 Effect of temperature stress on plants

TABLE 2.1 Showing symptoms in various plants due to temperature stress and their protective mechanism of action. S. no. Plant name 1.

Saccharum officinarum

2.

Oryza sativa

3.

Brassica juncea

4.

Vitis vinifera

5.

Common name

Symptom

Sugarcane Reduced chlorophyll content, lower stomatal conductance, and reduced photosynthesis

Protective action against stress References Inhibited the generation of H2O2, improved K1 and Ca21 contents, and increased ABA response

Hasanuzzaman et al. (2013)

Inhibits the rates of pollen and spikelet fertility and affects the plant at the heading stage reduced the grain size and weight. But at low temperature stress, the symptom includes swelling of mitochondrial, thylakoid, and chloroplast membrane. Reduction in size, number, and weight of grains

Decreased electrolyte osmosis, reduced production rate of oxidative stress biomarkers, increase in cytosolic calcium, and activated signal transduction pathway, and transcription factors

Rahman et al. (2009)

Severely affects the plant at flowering and reproductive stage

Decreased seedling mortality, increased growth

Hasanuzzaman et al. (2013)

Grape vine

Reduced photosynthetic rate, abnormal stomatal closure

Enhanced Rubisco activity and Kepova et al. improved PSII photochemistry, (2005) increased photosynthesis

Triticum aestivum

Wheat

Reduction in leaf size and area, reduction in number of spike, and reduction grains size and in yield

Enhanced response of Djanaguiraman antioxidant machinery reduced et al. (2010) lipid peroxides in root and shoot

6.

Solanum lycopersicum

Tomato

Yellowing of leaves and wilting, reduction in photosynthesis rate membrane damage, cytological changes, metabolic dysfunction, i.e., unconversion of starch

Increase expression of stress Hasanuzzaman responsive gene, signal et al. (2013) transduction of hormone pathways genes, and decreased oxidative stress

7.

Solanum melongena

Brinjal

Electrolyte leakage, increase in proline content, damage to cell membranes, oxidative stress, and damage permeability of cell membrane

Synthesis of antioxidants glutathione, ascorbate, carotenoids, flavonoids, polyphenols, tocopherols, and ROS decomposing enzymes

8.

Nicotiana tabacum

Tobacco plants

Reduced photosynthetic rate, impaired stomatal conductance, and also reduced quantum yield of photosynthesis. Reduced antioxidant responses

Activation of antioxidant Hasanuzzaman defense system APX, CAT, and et al. (2013) POD

9.

Arabidopsis thaliana

Rice

Mustard

Thale cress

During seedling stage, Through NO production and excessive heat stress inhibit the activated signal transduction process of seed germination

Se˛kara et al. (2012)

MonteroBarrientos et al. (2010) (Continued)

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2. Regulation of temperature stress in plants

TABLE 2.1 (Continued) S. no. Plant name

Common name

Symptom

Protective action against stress References

10. Daucus carota

Carrot

Affects the plant at seedling Synthesis of HSP and stress stage and weaken the seed, hormone responses during germination it develops lesions

11. Zea mays

Maize

Activation of various signal Severely damages the plant Zhang et al. transduction molecules, related (2013) and ear growth rates, usually to stress responsive gene affects the plant during preanthesis and silking process Impairs the synthesis of hemicellulose and cellulose, which suppresses the cob extensibility. Chilling stress reduces ear expansion, reduction in yield, severe damage to plasma membrane and its disruption

12. Cicer arietinum

Gram

Reduced growth, reduction in Chl content and photosynthesis

Enhanced growth and less formation of reactive oxygen species, decreased melanoaldehyde (MDA) and H2O2 contents, improved water, and Chl content

Kumar et al. (2012)

13. Phragmites communis

Reed

Excessive oxidative stress and membrane damage, and damages to structural proteins and reduction in yield

Song et al. (2006)

14. Phaseolus vulgaris

Green bean

Damages at early stages of development and reduced growth rate and reduction in yield. But in chilling stress, plants show symptom such as desiccation of foliage, necrosis, spot on leaves, fruits, and at extreme condition death of a part of plant

Increased activities of enzymatic antioxidants such as SOD, CAT, APX, and POD which combat the generating ROS Increased activity of enzymatic antioxidants, such as CAT, GST, and POD, gene induction in response to cold CBF pathway

15. Abelmoschus esculentus

Okra

Reduces the production yield, damages and lowers the fiber content, and breaks down the calcium pectate

Activation of stress regulating gene and heat-shock proteins and antioxidant system for lesser damage to plants

Gunawardhana and de Silva (2011)

Enhanced antioxidant system, reduced oxidative stress lesser damage to membrane system, reduced leakage

Tan et al. (2011)

16. Glycine max

Soya bean Decreases the leaf area and stomatal aperture, damages the plasma membrane, and increases the thicknesses of the palisade and spongy layers, distortion of thylakoid, and organelle molecule

Lee et al. (2000)

El-Bassiony et al. (2012)

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2.2 Effect of temperature stress on plants

TABLE 2.1 (Continued) S. no. Plant name

Common name

17. Capsicum annum

Green chilly

18. Hordeum vulgare

Sorghum

19. Pisum sativum

Pea

20. Cucumis sativus

Symptom

Protective action against stress References

Reduces size and weight of fruits, produces abnormal seeds, and affects the plants during fruiting stage

Accumulation of osmoprotectant and enhanced antioxidant system

Cao et al. (2009)

Reduces pigment content Chla, affects PSII photochemistry and inhibits antioxidant enzyme activity, and increases oxidative stress and thylakoid membrane damage and reduction in yield

Decreased membrane damage and lipid peroxidation and enhanced antioxidant defense system, enhanced growth, and increased grain yield

Mohammed and Tarpley (2010)

Reduced size and number of pod, leaf senescence, and oxidative stress damage

Increased antioxidant response and activation of heat-shock proteins

Hall (2001)

Activation of several antioxidant and reduced oxidative stress, which maintain structural organization

Zhang et al. (2013)

Cucumber Damages to plasma membrane and increased permeability, electrolyte leakage, lipid peroxidation

21. Ipomea batata

Sweet potato

Physiological changes, changes Lowers the efficiency of ice in membrane structure, and nucleation sites, balances the structural proteins, decreased osmotic potential stomatal aperture and oxidative stress

22. Gossypium barbadense

Cotton

Degradation of polymeric protein into simple soluble forms, leading to the premature leaf senescence and leaf yellowing, reduced growth, increased ROS production and lipid peroxidation

23. Ananas comosus

24. Solanum tuberosum

Increased ABA responses and hormonal regulation reduced damage to lipid peroxidation

Pineapple Decreased CO2 exchange, CBF pathway that provides reduction in photosynthesis resistance under cold stress and degradation of chlorophyll pigment Potato

Reduced plant growth and promotes death, surface lesion, and discoloration and loss of vigor

Increase in cytosolic calcium which activates signaling components, ultimately leads to change in gene expression

Hasanuzzaman et al. (2013)

Hasanuzzaman et al. (2013)

Alden and Hermann (1971)

Hasanuzzaman et al. (2013)

(Continued)

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2. Regulation of temperature stress in plants

TABLE 2.1 (Continued) S. no. Plant name

Common name

Symptom

Protective action against stress References

25. Musa acuminata

Banana

Reduction in growth, reduced photosynthesis, and low performance of PSII photochemistry and generation of reactive oxygen species, which leads to membrane damage, browning of skin, and rescinding of pulp tissue

Activation of antioxidative enzymes and reduced oxidative stress, activation of transcription factors, and signal transduction pathway

Zhang et al. (2012)

26. Plectranthus scutellarioides

Coleus

Swelling up of mitochondria chloroplast and membrane bound organelle, damage to protein and lipid, inhibited growth, decrease in photosynthesis and respiration

Maintain cell fluidity, ABA stress hormone responses and enhanced antioxidant system, which improves growth and the PSII photochemistry

Lyons (1973)

Transcription factors CBF activates, which in turn activate stress response gene, reduced oxidative damage

Reid (1991)

27. Passiflora incarnata

Passiflora Cracking of stem, reduced plant growth and death, abnormal curling Swelling up of mitochondria chloroplast and membrane bound organelle, damage to protein and lipid, inhibited growth, decrease in photosynthesis and respiration

ABA, Abscisic acid; APX, ascorbate peroxidase; CAT, catalase; CBF, C-repeat binding factor; GST, glutathione S-transferase; HSP, heat-shock proteins; POD, peroxidase; PSII, photosystem II; ROS, reactive oxygen species; SOD, superoxide dismutase.

called primary and secondary events. Primary symptom causes membrane phase transition from liquid to the solid gel phase; this, in turn, decreases the membrane permeability, that is, fluidity, and promotes the expression of secondary symptom. Although enzymes are more labile to high-temperature stress, low temperature also affects the enzyme efficiency. Several enzymes of metabolic process, such as pyruvate P1 dikinase and phosphofructokinase, which serve important role in carbon fixation reactions in C4 plants and glycolysis, respectively, are more affected by chilling temperature as they alter the structure of enzyme. K-mediated ATPase also affected by low temperature as the repressed activity leads to the leakage of K ion from cells. Enzyme kinetics is also altered by chilling stress as it causes reduced reaction velocity (Vmax) and the affinity (Km) of the enzyme for its substrate (Hussain et al., 2018). The adenine nucleotides, that is, adenosine triphosphate (ATP), ADP, and AMP, are also reduced by chilling stress. Photosynthesis and respiration are also affected by cold stress as it affecting both the light and dark reactions; it causes photoinhibition at the oxidative side of PSII involving D1 protein (Kreps et al., 2002). Chilling stress disrupts the normal electron transport chain leading to the leakage of electrons, which generates ROS that causes oxidative stress and degrades the membrane. Duration of the chilling stress causes respiration rate to increase or decrease, as short period increases the respiration rate because normal electron

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transport chain diverts to the cyanide-resistant pathway, while long-term or very low temperature causes cell damage and death and also decreases the rates.

2.3 Plant adaptations to heat stress On the basis of temperature, plants are being categorized into three groups: (1) psychrophiles, which grow optimally at low temperature ranging between 0
C and 10
C; (2) mesophyles, favor moderate temperature ranging between 10
C and 30
C; and (3) thermophilies, which raise well in temperature between 30
C and 65
C or even in higher ´ ´ bek-Sokolnik, 2012). There is a great disparity among the plant species in rapports of (Zro their resistant behavior and tolerance to heat stress.

2.3.1 Physiological adaptation Under temperature stress, plants evolve two types of responses, one is long-term response that falls under (evolutionary, phonological, and morphological adaptations) and the other is short-term (avoidance or acclimation) response. Plants exhibited several physiological changes including alteration in leaf orientation, change in composition of membrane lipids, or increase the transpirational cooling. Leaves of plants are very labile to temperature, and under stress condition, leaves closed the stomata, increased the stomatal, trichomatous densities, and in vascular bundle, xylem vessels become larger to avoid heat stress (Srivastava et al., 2012). Plants under extreme high-temperature environment avoid excess temperature by reducing the absorption of solar radiation by the presence of thick cuticle having small hairs (tomentose) and waxy covering. Leaf orientation also changed under changing temperature of environment as leaf blades turn away from light and change their orientation by rolling in such a way that they seem to be parallel with falling sun rays (Hasanuzzaman et al., 2013). In general, temperature tolerant species having small-sized leaves than temperature sensitive species and avoid heat stress. The increasing rate of transpiration is also a strategy of plants to maintain basal temperature, and it protects leaves from heat stress and temperature that is around 6
C lower than outside temperature (Fitter and Hay, 2002). Plant life cycle also modified in response to temperature as leaf abscission, dessert annuals and increasing the heat resistant buds, and completes their reproductive phase in cooler months to avoid heat stress (Fitter and Hay, 2002). Sarieva et al. (2010) studied that under heat stress condition, wheat leaves show a significant increase in water metabolism. Although all plants in their early life cycle are sensitive to temperature, resistance toward high temperature develops in summer environment and the highest level of tolerance during winter dormancy. To avoid damage due to temperature stress, proper sowing methods play very important role, such as choice of sowing date, cultivars, and irrigation methods. Further, lettuce plant seeds when grown in summer show improper germination and shows proper germination by sowing the lettuce seed into dry beds during the day and then sprinkle irrigating the beds during the late afternoon. To avoid improper germinations, seeds of different plants are kept in osmotic solution to provide constant temperature for several days. Furthermore, tolerance strategy

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2. Regulation of temperature stress in plants

FIGURE 2.2 Schematic diagram showing alteration in plants due to temperature stress at different level.

was also an adaptive response against temperature stress, which includes production of osmoprotectants, late embryogenesis abundant proteins, increase in ion transporters, and involvement of antioxidant defense system (Rodrı´guez et al., 2005; Wang et al., 2004). In response to the applied stress types, different plant parts show variation in developmental complexity (Queitsch et al., 2000). Changes in membrane fluidity under temperature stress reestablish homeostasis and to protect and repair damaged proteins and membranes (Vinocur and Altman, 2005) (Fig. 2.2).

2.3.2 Biochemical adaptation Generation of oxidative stress biomarkers is common end point to evaluate the toxicity induced by abiotic stresses. To cope with damaging effects caused by ROS, every organism has an array of antioxidants machinery, which include the SOD, CAT, ascorbate peroxidase (APX), monodehydroascorbate reductase, dehydroascorbate reductase, glutathione reductase (GR), GST, glutathione peroxidase (GPX), and POD and nonenzymatic compounds, such as ascorbate (AsA), glutathione (GSH), and carotenoids (Gill and Tuteja, 2010; Singh et al., 2016). However, excessive ROS generation leads to cell death due to inhibition in normal cell division. Role of ROS depends on its concentrations; at low

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2.3 Plant adaptations to heat stress

35

concentrations, these ROS act as signaling molecules that activate the signal cascades, while at higher concentrations, it is toxic to cell (Singh et al., 2016). Tolerance against temperature stress is related with an enhanced antioxidative capacity (Babu and Devraj, 2008). Studies suggest that heat acclimated plant species having low ROS generation due to excessive synthesis of AsA and GSH (Xu et al., 2006). Studied antioxidant enzymes are temperature sensitive, which under extreme temperature inactivate the enzymes, while these antioxidant enzymes are also activate with increasing temperature. At 50
C, enzymes such as CAT, APX, and SOD were found to accelerate initially but declined after longterm exposure, while POD and GR were found to decrease under temperature ranging from 20
C to 50
C (Chakraborty and Pradhan, 2011). Overall antioxidant status was maximum in temperature tolerant species under 35
C40
C, while in sensitive species, it was maximum at 30
C and depended upon species to species (Chakraborty and Pradhan, 2011). In chloroplast and mitochondria, super oxide radicle (SOR) is continuously synthesized due to leakage of electrons, and for scavenging of SOR, cells have SOD (considered as first line of defense) that dismutates the SOR into H2O2. Further, APX, CAT, and POD are actively involved in scavenging of H2O2. In cells due to presence of Fe21 and Fe31, H2O2 forms the hydroxyl radicle via HaberWeiss reaction, which is very toxic among ROS (Gill and Tuteja, 2010) and subsequently damages the membrane, proteins, DNA, lipids, and other important macromolecules (Singh et al., 2016). Furthermore, metabolites (nonenzymatic antioxidants) such as AsA, GSH, tocopherol, cysteine, proline, and carotene also confer the tolerance against temperature stress (Sairam et al., 2000). According to Xu et al. (2006), heat-tolerant turf grass and wheat showed enhanced amount of AsA and GSH, which leads lower ROS production. Similarly, Balla et al. (2009) confirmed that the antioxidative enzyme system plays a very important role in defense against heat stress. The enhanced activity of the enzymes GST, APX, and CAT was recorded to be more in the cultivar, which showed better resistance to heat stress and prognosis against ROS production (Singh et al., 2016). In general, an increase in temperature leads to an increased expression of the antioxidative enzymes until a particular temperature after which they decline. The temperature until which increased activities are maintained varies in the tolerant and susceptible varieties.

2.3.3 Molecular adaptation Under adverse environmental factors, plants have evolved several mechanisms allowing them to grow in such environment and enhance the crop productivity by increasing its survivability. Under stress condition, plants activated specific ion channels and kinase cascades along with overexpression of stress hormone, such as abscisic acid, ET, salicylic acid, and jasmonic acid and reprograming of the genetic machinery results in adequate defense reactions (Fujita et al., 2006). Plants tolerate temperature stress by modulating genes and also regulate the gene expression involve in activation HSPs (Vinocur and Altman, 2005). Majority of stress tolerance proteins are soluble in water and among them, HSPs are exclusively concerned in heat-stress response. HSPs are enormously heterogenous proteins, and their expression is occurred during early developmental events, such as seed germination, embryogenesis, microsporogenesis, and fruit set (Prasinos et al., 2005). HSPs were found to

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2. Regulation of temperature stress in plants

increase under high temperature and first reported in an insect Drosophila melanogaster and other stress factors, such as azide, salicylate, and 2,4-dinitrophenol, also upregulate the expression of HSPs (Al-Wahibi, 2011). Furthermore, HSPs synthesis was reported in Glycine max seedlings exposed with variation of temperature from 28
C to 45
C for 10 minutes and longer duration kills the seedlings (Lin et al., 1984). All HSPs share common structure having carboxylic terminal called heat-shock domain (Helm et al., 1993), and its weight ranges from 10 to 200 kDa and assigned as chaperones that actively participate in induction of signals under heat stress. In eukaryotes including plants, five different families of HSPs are reported, such as HSP100 (or ClpB), HSP90, HSP70 (or DnaK), HSP60 (or GroE), and HSP 20 [or small HSP (sHSP)] (Swindell et al., 2007). Among these HSPs, HSP70 and HSP60 play important role in heat stress tolerance and highly conserved throughout the plant species (Kulz, 2003). According to Vierling (1991), around 20 types of HSPs are reported, and sometimes it is up to 40 and maximum diversity was found in sHSPs (Morrow and Tanguay 2012) having molar mass of 1240 kDa (Wang et al., 2004). In plant cell, major site for HSPs productions are cell wall, chloroplasts, mitochondria, and ribosomes (Nieto-Sotelo et al., 2002; Yang et al., 2006) and differ among different plants, such as five mitochondrial LMW-HSPs (28, 23, 22, 20, and 19 kDa) were expressed in maize and only one (20 kDa) in wheat and rye under 40
C temperature suggesting high tolerance nature of maize against heat stress (Korotaeva et al., 2001). In general, HSPs protect the proteins from denaturation and behave as thermo-protectant. Double-stranded DNA sequences having promoter region in which conserved heat-shock elements (HSEs) induce the expression of heat-shock transcription factors or simply heat-shock factors (HSFs) (Nover et al., 2001). Heat upregulates the HSFs, which is involved in synthesis of particular heat stress tolerant gene that depends on intensity and timing of stress. In Arabidopsis thaliana, APX gene (APX1) also has HSE in its 50 -promoter region that protects plants against heat stress. HSPs in aggregation form chaperones and promotes proper protein folding, targeting, and maturation of proteins as well as involve in protein renaturation and stabilized the membrane (Torok et al., 2001). Furthermore, genetic engineering is implicated to develop more thermotolerance plants known as transgenic plants (Rodrı´guez et al., 2005), in which overexpression of sHSPs/chaperones and manipulation of HSF gene occurred. Transgenic HT stress tolerant Arabidopsis was produced by transformed expression of HSPs by making changes in transcription factor (AtHSF1) responsible for induction of HSPs (Lee et al., 1995). Similarly, in transgenic rice plants, there is overexpression of Arabidopsis Hsp101 and induce the sHSP17.7 gene suggests its better role in heat tolerance (Torok et al., 2001; Murakami et al., 2004). Apart from this, a number of other plant proteins, which are activated and triggered/stimulated upon heat stress including ubiquitin (Sun and Callis, 1997), cytosolic Cu/Zn-SOD (Herouart and Inze´, 1994), and Mn-POD (Shah and Nahakpam, 2012). A recent branch of science, that is, “omics,” gives new prospects and hopes for the identification of various signaling pathway, molecular mechanism such as transcriptional and translational modifications that regulate the responses in plant against stress condition (Aprile et al., 2009) (Fig. 2.3).

2.3.4 Nutrient management approach To fulfill the food demand of the burgeoning population of the world, which is expected to reach up to 10 million by the end of year 2050, various approaches are applied Plant Life under Changing Environment

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FIGURE 2.3 Schematic diagram showing generation of reactive oxygen species and their site of action and regulation of oxidative stress.

in agricultural field against biotic and abiotic factors to increase the crop productivity. Among them, plant nutrients, including macro- and micronutrients, are considered as important strategies to alleviate temperature stress (Waraich et al., 2011). According to Cakmak (2002), around 60% of cultivated lands are mineral-nutrient deficient soil due to unbalance and inadequate supply of mineral nutrients, thereby limiting the food production in developing countries. Furthermore, proper nutrients are key components that actively participate in various physiological and biochemical activities, such as magnesium (Mg) is involved in chlorophyll synthesis and participates in photosynthesis, phosphorous (PO22 4 ) is needed for energy production as well as core component of nucleic acids (Waraich et al., 2011), and many more participate in growth and development of plants. Therefore more biomass production is achieved in well-nourished plans compared to unwell-nourished ones. A lot of work has been done in this area where nutrient management approach significantly alleviates the negative effects of any kind of stress. Tolerance in wheat is increased by application of silicon (Si) and potassium (K) (Munns, 2005; Tahir et al., 2011). 2.3.4.1 Role of macronutrients Macronutrients are chemical elements or substances (such as potassium or protein) that are crucial and fairly required in large amounts for the growth and development of a Plant Life under Changing Environment

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2. Regulation of temperature stress in plants

living organism. They basically include carbon (C), hydrogen (H), phosphorus (P), potassium (K), nitrogen (N), and sulfur (S), which are building blocks for living organism. Among macronutrients, nitrogen (N) plays a prominent role in utilization of energy and photosynthetic carbon reduction (CO2 fixation) cycle and alleviates the negative effects induced by high and low temperature (Huang et al., 2004). Increases in ambient temperature significantly affect the nutrient uptake and negatively affect the developmental process. Nitrogen-deprived leaves show photoinhibition of photosynthetic apparatus because excess light energy was not utilized by plant leaves associated with increased damage to lipid bilayer (Huang et al., 2004). In the finding of Kato et al. (2003), it was stated that plants supplemented with excess N show tolerance toward high light compared to those plants which were grown under limited N supply due to that absorbed light energy is actively involved in photosynthetic electron transport chain. These results clearly described the role of N in improving the photosynthesis under high temperature and develop protective mechanisms as excess light is dissipated in form of heat. Furthermore, N also involved in light-dependent xanthophyll cycle that involved in protection against photo-oxidative damage (Demming-Adams and Adams, 1996). Fertilizers that contain N as a major proportion significantly mitigate the negative effects caused by abiotic factors (Waraich et al., 2011). In plants, N as nitric oxide (NO) is a free radical gaseous molecule that actively mediating the responses to heat stress (Zhang et al., 2006) and involved in various biological functions (Domingos et al., 2015) by diffusing across the biological membranes (Yu et al., 2014). Various physiological processes such as seed germination, plant maturation and senescence (Mishina et al., 2007), and stress tolerance (Ziogas et al., 2013) are mediated by NO signaling. Besides, NO-mediated plant heat tolerance includes decreasing ROS generation, produces osmolyte, and involves in hormonal-mediated signaling events. Accumulation of NO is reported in several plants under high-temperature treatments (Yu et al., 2014) and explained its vital role in adaptation against stress tolerance (Bouchard and Yamasaki, 2008), and it depends on time interval, that is, cells exhibited less NO surge at 35
C compared to cells exposed to 55
C temperature (Locato et al., 2008). Short-term exposure of cells with high temperature associated with increased NO production in leaves and diverse cell types, such as palisade mesophyll cells or epidermal cell types, guard cells, and subsidiary cells of Nicotiana tobacum, Medicago sativa, and in Pisum sativum (Leshem, 2001; Gould et al., 2003; Chaki et al., 2011). According to Uchida et al. (2002), it was demonstrated that NO protected the chloroplast against oxidative damage under heat stress by inducing expression of gene encoding sHSP26. Furthermore, potassium (K) is involved in various physiological processes, such as photosynthesis, activation of enzymes, and translocation of photosynthates, into sink and enhances the tolerance mechanism against adverse environmental factors (Mengel and Kirkby, 2001). Chilling-induced photo-oxidative damage can be enhanced under low K in plants and adequate supply of K in soils can improve the growth of plants exposed to chilling stress by minimizing the oxidative stress and providing defense against stem damage after low night temperature in carnation plants (Kafkafi, 1990). Similar results were also obtained in potato, tomato, pepper, and eggplant where K fertilizers alleviate the chilling-induced adverse effects (Grewal and Singh, 1980). A number of physiological processes and secondary signaling are mediated by calcium (Ca) and act as secondary messenger (Waraich et al., 2011). Calcium plays a vital role in arbitrating stress response

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during cold injury, recovery from damage, and acclimation to cold strain (Palta, 2000), and it is a necessary element in plants for recovery from low-temperature stress by inducing the plasma membrane enzyme ATPase that is required to pump back the nutrients that were lost during cell damage (Palta, 2000) and maintain the cell structure. Since dehydration is the common denominator, Ca also plays a role as calmodulin that switches the plant metabolic reactions and boosts the plant growth under low-temperature stress condition. Likewise calcium, magnesium (Mg) is also involved in different physiological and biochemical processes of plants as it sways the course of growth and development in plants (Waraich et al., 2011) and a major constituent of photosynthetic pigments particularly chlorophyll and participates in photosynthesis and plays an important role in electron transport chain in chloroplast. In electron transport chain (ETC), it participates in energy transfer between photosystem II and nicotinamide adenine dinucleotide phosphate (NADP1) and protects thylakoid against oxidative damage (Halliwell and Gutteridge, 1999). Mg also involved in upregulation of enzymatic antioxidants that minimize the toxicity induced by ROS in bean (Cakmak, 1994), maize (Tewari et al., 2004), pepper (Anza et al., 2005), and mulberry (Tewari et al., 2006). The photosynthetic rate is also enhanced by maintenance of chloroplast structure by improving Mg nutrition. 2.3.4.2 Role of micronutrients Micronutrients are chemical elements or substances (such as potassium or protein) that are necessary in relatively small amounts for the better functioning of the growth and development of plants; they include boron (B), manganese (Mn), selenium (Se), chlorine (Cl), copper (Cu), iron (Fe), zinc (Zn), and molybdenum (Mo). Boron (B) vigorously participates in cell elongation, cell wall biosynthesis, cell division, nitrogen metabolism, and leaf biosynthesis. Chilling or heat stress significantly enhances the level of ROS, such as SOR, H2O2, and hydroxyl radical, and causes cell injury due to accumulation inside the cell associated with membrane damage (Molassiotis et al., 2006). Boron upsurges the antioxidant capacity of plants and thus alleviates ROS damage induced by temperature stress as well as enhances the sugar transport in plants and in germinating seeds. Boron also enhances the photosynthetic activity of plants-exhibited temperature stress. Furthermore, temperature stress significantly reduces the nutrient uptake in plants and adequate supply of nutrients improves the growth. Besides its direct role, Mn indirectly reduces the adverse effects caused by temperature stress by enhancing the efficacy of photosynthesis and nitrogen metabolism process of plant cell. Mn is an integral part of oxygen evolving complex, and Mn supply improves the electron flow in ETC and reduces the chlorosis in leaves and also involved in the activation of antioxidants under temperature stress (Aloni et al., 2008). Selenium (Se) is a trace element basically involved in activation of enzymatic antioxidants particularly GPX and required in very low concentrations and protects plants from abiotic stresses (Valadabadi et al., 2010). Selenium deficient plants exhibited enhanced lipid peroxidation (Valko et al., 2005), and Se supply significantly prevents the oxidative damage (Lobanov et al., 2008). Xue et al. (2001) reported that plants grown under high-temperature stress when treated with selenium showed less senescence-related oxidative stress and maintained green leaf color for an extensive period.

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2. Regulation of temperature stress in plants

2.4 Conclusion Plants in their life cycle face adverse environmental factors, including biotic and abiotic. Among these, temperature stress (low and high) is an important factor that directly or indirectly influences the growth and development of plants. Temperature stress affects the plant at different levels, such as at morphological, biochemical, and molecular, and degree of toxicity is different in plants facing low and high temperature. High temperature enhances the denaturation of enzymes and proteins and also denatures the DNA structure at molecular level and loss of membrane integrity. On the other hand, low temperature particularly affects the reproductive fitness of plants, ovule abortion, and reduced fruit set. Due to these adverse impacts, it is necessary to increase the protective mechanism against temperature stress. Plants develop several strategies at morphological, biochemical, and molecular levels to cope up with temperature stress. At morphological level, avoidance and tolerance mechanism is adopted. ROS generation is a common phenomenon by temperatures stress. To mitigate ROS-induced damage, every plant having an array of antioxidant machinery includes enzymatic (SOD, POD, CAT, and GST) antioxidants. Besides, HSP is common protein that is involved in heat stress tolerance, including HSP 60 and 90. The management of plant nutrients is very helpful to develop plant tolerance to temperature stress. Better plant nutrition can effectively alleviate the adverse effects of temperature stress by numerous mechanisms. Application of nutrients such as N, Ca, Mg, B, K, and Se reduced the ROS by enhancing the antioxidant system. Nutrient management significantly enhances the crop productivity for the betterment of human welfare.

References Abuqamar, S., Luo, H., Laluk, K., Mickelbart, M.V., Mengiste, T., 2009. Crosstalk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor. Plant J. 58, 347360. Ahamed, K.U., Nahar, K., Fujita, M., Hasanuzzaman, M., 2010. Variation in plant growth, tiller dynamics and yield components of wheat (Triticum aestivum L.) due to high temperature stress. Adv. Agric. Bot. 2, 213224. Alden, J., Hermann, R.K., 1971. Aspects of the cold-hardiness mechanism in plants. Bot. Rev. 37, 37142. Aloni, B., Karni, L., Deventurero, G., Turhan, E., Aktas, H., 2008. Changes in ascorbic acid concentration, ascorbate oxidase activity, and apoplastic pH in relation to fruit development in pepper (Capsicum annuum L.) and the occurrence of blossom-end rot. J. Hortic. Sci. Biotechnol. 83, 100105. Al-Wahibi, M., 2011. Plant heat-shock proteins: a mini review. J. King Saud Univ. Sci. 23, 139150. Anza, M., Riga, P., Garbisu, C., 2005. Time course of antioxidant responses of Capsicum annuum subjected to progressive magnesium deficiency. Ann. Appl. Biol. 146, 123134. Aprile, A., Mastrangelo, A.M., De Leonardis, A.M., Galiba, G., Roncaglia, E., Ferrari, F., et al., 2009. Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genomics 10, 279. Babu, N.R., Devraj, V.R., 2008. High temperature and salt stress response in French bean (Phaseolus vulgaris). Aust. J. Crop Sci. 2, 4048. Balla, K., Bencze, S., Janda, T., Veisz, O., 2009. Analysis of heat stress tolerance in winter wheat. Acta Agron. Hung. 57, 437444. Baxter, A., Mittler, R., Suzuki, N., 2014. ROS as key players in plant stress signalling. J. Exp. Bot. 65, 12291240. Bolton, M.V., 2009. Primary metabolism and plant defense—fuel for the fire. Mol. Plant Microbe Interact. 22, 487497. Bouchard, J.N., Yamasaki, H., 2008. Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: a possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol. 49, 641652.

Plant Life under Changing Environment

References

41

Cakmak, I., 1994. Activity of ascorbate-dependent H2O2-scavenging enzymes and leaf chlorosis are enhanced in magnesium and potassium-deficient leaves, but not in phosphorus-deficient leaves. J. Exp. Bot. 45, 12591266. Cakmak, I., 2002. Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant Soil 247, 324. Cao, Y.Y., Duan, H., Yang, L.N., Wang, Z.Q., Liu, L.J., Yang, J.C., 2009. Effect of high temperature during heading and early filling on grain yield and physiological characteristics in indica rice. Acta Agron. Sin. 35, 512521. Chaki, M., Valderrama, R., Ferna´ndez-Ocan˜a, A.M., Carreras, A., Go´mez-Rodrı´guez, M.V., Lo´pez-Jaramillo, J., 2011. High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxinNADP reductase by tyrosine nitration. Plant Cell Environ. 34, 18031818. Chakraborty, U., Pradhan, D., 2011. High temperature-induced oxidative stress in Lens culinaris, role of antioxidants and amelioration of stress by chemical pre-treatments. J. Plant Interact. 6, 4352. Demming-Adams, B., Adams III, W.W., 1996. The role of the xanthophyll cycle carotenoids in protection of photosynthesis. Trends Plant Sci. 1, 2126. Djanaguiraman, M., Sheeba, J.A., Devi, D.D., Bangarusamy, U., 2009. Cotton leaf senescence can be delayed by nitrophenolate spray through enhanced antioxidant defense system. J. Agron. Crop Sci. 195, 213224. Djanaguiraman, M., Prasad, P.V.V., Seppanen, M., 2010. Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system. Plant Physiol. Biochem. 48, 9991007. Domingos, P., Prado, A.M., Wong, A., Gehring, C., Feijo, J.A., 2015. Nitric oxide: a multitasked signaling gas in plants. Mol. Plant 8, 506520. El-Bassiony, A.M., Ghoname, A.A., El-Awadi, M.E., Fawzy, Z.F., Gruda, N., 2012. Ameliorative effects of brassinosteroids on growth and productivity of snap beans grown under high temperature. Gesunde Pflanz. 64, 175182. Fedoroff, N.V., Battisti, D.S., Beachy, R.N., Cooper, P.J., Fischhoff, D.A., Hodges, C.N., et al., 2010. Radically rethinking agriculture for the 21st century. Science 327, 833834. Fitter, A.H., Hay, R.K.M., 2002. Environmental Physiology of Plants, third ed. Academic Press, London, UK. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., 2006. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signalling networks. Curr. Opin. Plant Biol. 9, 436442. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909930. Gould, K.S., Lamotte, O., Klinguer, A., Pugin, A., Wendehenne, D., 2003. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26, 18511862. Greer, D.H., Weedon, M.M., 2012. Modelling photosynthetic responses to temperature of grapevine (Vitis vinifera cv. Semillon) leaves on vines grown in a hot climate. Plant Cell Environ 35, 10501064. Grewal, J.S., Singh, S.N., 1980. Effect of potassium nutrition on frost damage and yield of potato plants on alluvial soils of the Punjab. Plant Soil 57, 105110. Gunawardhana, M.D.M., de Silva, C.S., 2011. Impact of temperature and water stress on growth yield and related biochemical parameters of okra. Trop. Agric. Res. 23, 7783. Guy, C., Kaplan, F., Kopka, J., Selbig, J., Hincha, D.K., 2008. Metabolomics of temperature stress. Physiol. Plant. 132, 220235. Hall, A.E., 2001. Crop Responses to Environment. CRC Press LLC, Boca Raton, FL. Halliwell, B., Gutteridge, J.M.C., 1999. Free Radicals in Biology and Medicine, third ed. Oxford University Press, Oxford, UK. Hasanuzzaman, M., Hossain, M.A., da Silva, J.A.T., Fujita, M., 2012. Plant responses and tolerance to abiotic oxidative stress: antioxidant defenses is a key factor. In: Bandi, V., Shanker, A.K., Shanker, C., Mandapaka, M. (Eds.), Crop Stress and Its Management: Perspectives and Strategies. Springer, Berlin, Germany, pp. 261316. Hasanuzzaman, M., Nahar, K., Md, M.A., Chowdhury, R.R., Fujita, M., 2013. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 14, 96439684. Helm, K.W., Lafayete, P.R., Nago, R.T., Key, J.L., Vierling, E., 1993. Localization of small heat shock proteins to the higher plant endomembrane system. Mol. Cell. Biol. 13, 238247.

Plant Life under Changing Environment

42

2. Regulation of temperature stress in plants

Herouart, D.V.M.M., Inze´, D., 1994. Developmental and environmental regulation of the Nicotiana plumbaginifolia cytosolic Cu/Zn-superoxide dismutase promoter in transgenic tobacco. Plant Physiol. 104, 873880. Huang, Z.A., Jiang, D.A., Yang, Y., Sun, J.W., Jin, S.H., 2004. Effects of nitrogen deficiency on gas exchange, chlorophyll fluorescence, and antioxidant enzymes in leaves of rice plants. Photosynthetica 42, 357364. Hussain, H.A., Hussain, S., Khaliq, A., Ashraf, U., Anjum, S.A., Men, S., et al., 2018. Chilling and drought stresses in plants: implication, cross talk, and potential management opportunities. Front. Plant Sci. 9, 393. Available from: https://doi.org/10.3389/fpls.2018.00393. Kafkafi, U., 1990. Impact of potassium in relieving plants from climatic and soil-induced stresses. In: Johnston, A. E. (Ed.), Food Security in the WANA Region, the Essential Need for Balanced Fertilization. International Potash Institute, Basel, pp. 317327. Kato, M.C., Hikosaka, K., Hirotsu, N., Makin, A., Hirose, T., 2003. The excess light energy that is either utilized in photosynthesis nor dissipated by photoprotective mechanisms determines the rate of photoinactivation in photosystem II. Plant Cell Physiol. 44, 318325. Kepova, K.D., Holzer, R., Stoilova, L.S., Feller, U., 2005. Heat stress effects on ribulose-1,5-bisphosphate carboxylase/oxygenase, Rubisco binding protein and Rubisco activase in wheat leaves. Biol. Plant. 49, 521525. Kim, D.H., Doyle, M.R., Sung, S., Amasino, R.M., 2009. Vernalization: winter and the timing of flowering in plants. Annu. Rev. Cell Dev. Biol. 25, 277299. Kira´ly, L., Hafez, Y.M., Fodor, J., Kira´ly, Z., 2008. Suppression of Tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with down regulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. J. Gen. Virol. 89, 799808. Korn, M., Ga¨rtner, T., Erban, A., Kopka, J., Selbig, J., Hincha, D.K., 2010. Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol. Plant 3, 224235. Korotaeva, N.E., Antipina, A.I., Grabelynch, O.I., Varakina, N.N., Borovskii, G.B., Voinikov, V.K., 2001. Mitochondrial low-molecular-weight heat shock proteins and tolerance of crop plant’s mitochondria to hyperthermia. Fiziol. BiokhimKul’turn. Rasten. 29, 271276. Krasensky, J., Jonak, C., 2012. Drought, salt and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 15931608. Kreps, J.A., Wu, Y., Chang, H.S., Zhu, T., Wang, X., Harper, J., 2002. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 21292141. Kulz, D., 2003. Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J. Exp. Biol. 206, 31193124. Kumar, S., Kaur, R., Kaur, N., Bhandhari, K., Kaushal, N., Gupta, K., et al., 2011. Heat-stress induced inhibition in growth and chlorosis in mungbean (Phaseolus aureus Roxb.) is partly mitigated by ascorbic acid application and is related to reduction in oxidative stress. Acta Physiol. Plant. 33, 20912101. Kumar, S., Kaushal, N., Nayyar, H., Gaur, P., 2012. Abscisic acid induces heat tolerance in chickpea (Cicer arietinum L.) seedlings by facilitated accumulation of osmoprotectants. Acta Physiol. Plant. 34, 16511658. Lee, J.H., Hubel, A., Schoffl, F., 1995. Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermo tolerance in transgenic Arabidopsis. Plant J. 8, 603612. Lee, B.H., Won, S.H., Lee, H.S., Miyao, M., Chung, W.I., Kim, I.J., et al., 2000. Expression of the chloroplastlocalized small heat shock protein by oxidative stress in rice. Gene 245, 283290. Leshem, Y.Y., 2001. Nitric Oxide in Plants. Occurrence, Function and Use. Kulwer Academic Publishers, Boston, MA. Lin, C.Y., Roberts, J.K., Key, J.L., 1984. Acquisition of thermo tolerance in soybean seedlings: synthesis and accumulation of heat shock proteins and their cellular localization. Plant Physiol. 74, 152160. Liu, H., Abudureheman, B., Zhang, L., Baskin, J.M., Baskin, C.C., Zhang, D., 2017. Seed dormancy breaking in a cold desert shrub in relation to sand temperature and moisture. AoB Plants. Available from: https://doi.org/ 10.1093/aobpla/plx003. Lobanov, A.V., Hatfield, D.L., Gladyshev, V.N., 2008. Reduced reliance on the trace element selenium during evolution of mammals. Genome Biol. 9, R62. Lobell, D.B., Asner, G.P., 2003. Climate and management contributions to recent trends in U.S. agricultural yields. Science 299. Available from: https://doi.org/10.1126/science.1078475.

Plant Life under Changing Environment

References

43

Locato, V., Gadaleta, C., De Gara, L., de Pinto, M.C., 2008. Production of reactive species and modulation of antioxidant network in response to heat shock: a critical balance for cell fate. Plant Cell Environ. 31, 16061619. Lyons, J.M., 1973. Chilling injury in plants. Ann. Rev. Plant Physiol. 24, 445466. Mengel, K., Kirkby, E.A., 2001. Principles of Plant Nutrition, Fifth ed. Kluwer Academic Publishers, Dordrecht. Mengiste, T., Chen, X., Salmeron, J., Dietrich, R., 2003. The Botrytis susceptible gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 5, 25512565. Mishina, T.E., Lamb, C., Zeier, J., 2007. Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant Cell Environ. 30, 3952. Mohammed, A.R., Tarpley, L., 2010. Effects of high night temperature and spikelet position on yield-related parameters of rice (Oryza sativa L.) plants. Eur. J. Agron. 33, 117123. Molassiotis, A., Sotiropoulos, T., Tanou, G., Diamantidis, G., Therios, I., 2006. Boron-induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh). Environ. Exp. Bot. 56, 5462. Montero-Barrientos, M., Hermosa, R., Cardoza, R.E., Gutie´rrez, S., Nicola´s, C., Monte, E., 2010. Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J. Plant Physiol. 167, 659665. Morrow, G., Tanguay, R.M., 2012. Small heat shock protein expression and functions during development. Int. J. Biochem. Cell Biol. 44, 16131621. Moury, B., Selassie, K.G., Marchoux, G., Daube`ze, A., Palloix, A., 1998. ). High temperature effects on hypersensitive resistance to Tomato spotted wilt to spovirus (TSWV) in pepper (Capsicum chinense Jacq.). Eur. J. Plant Pathol. 104, 489498. Munns, R., 2005. Genes and salt tolerance: bringing them together. Tansley review. New Phytol. 167, 645656. Murakami, T., Matsuba, S., Funatsuki, H., Kawaguchi, K., Saruyama, H., Tanida, M., et al., 2004. Overexpression of a small heat shock protein, sHSP17.7, confers both heat tolerance and UV-B resistance to rice plants. Mol. Breed. 13, 165175. Nieto-Sotelo, J., Martı´nez, L.M., Ponce, G., Cassab, G.I., Alago´n, A., Meeley, R.B., et al., 2002. Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. Plant Cell 14, 16211633. Nover, L., Bharti, K., Doring, P., Mishra, S.K., Ganguli, A., Scharf, K.D., 2001. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need. Cell Stress Chaperones 6, 177189. Palta, J.P., 2000. Stress interactions at the cellular and membrane levels. Hortic. Sci. 25, 111377. Prasinos, C., Krampis, K., Samakovli, D., Hatzopoulos, P., 2005. Tight regulation of expression of two Arabidopsis cytosolic Hsp90 genes during embryo development. J. Exp. Bot. 56, 633644. Qu, A.L., Ding, Y.F., Jiang, Q., Zhu, C., 2013. Molecular mechanisms of the plant heat stress response. Biochem. Biophys. Res. Commun. 432, 203207. Queitsch, C., Hong, S.W., Vierling, E., Lindquist, S., 2000. Hsp 101 plays a crucial role in thermo tolerance in Arabidopsis. Plant Cell 12, 479492. Rahman, M.A., Chikushi, J., Yoshida, S., Karim, A.J.M.S., 2009. Growth and yield components of wheat genotypes exposed to high temperature stress under control environment. Bangladesh J. Agric. Res. 34, 361372. Reid, M.S., 1991. Effects of low temperatures on ornamental plants. Acta Hortic. 298, 215224. Rodrı´guez, M., Canales, E., Borra´s-Hidalgo, O., 2005. Molecular aspects of abiotic stress in plants. Biotechnol. Appl. 22, 110. Ruelland, E., Vaultier, M.N., Zachowski, A., Hurry, V., 2009. Cold signalling and cold acclimation in plants. Adv. Bot. Res. 49, 35150. Sairam, R.K., Srivastava, G.C., Saxena, D.C., 2000. Increased antioxidant activity under elevated temperature: a mechanism of heat stress tolerance in wheat genotypes. Biol. Plant. 43, 245251. Sarieva, G.E., Kenzhebaeva, S.S., Lichtenthaler, H.K., 2010. Adaptation potential of photosynthesis in wheat cultivars with a capability of leaf rolling under high temperature conditions. Russ. J. Plant Physiol. 57, 2836.

Plant Life under Changing Environment

44

2. Regulation of temperature stress in plants

Se˛kara, A., Ba˛czek-Kwinta, R., Kalisz, A., Cebula, S., 2012. Tolerance of eggplant (Solanum melongena L.) seedlings to stress factors. Acta Agrobot. 65, 8392. Semenov, M.A., 2009. Impacts of climate change on wheat in England and Wales. J. R. Soc. Interface 6, 343350. Shah, K., Nahakpam, S., 2012. Heat exposure alters the expression of SOD, POD, APX and CAT isozymes and mitigates low cadmium toxicity in seedlings of sensitive and tolerant rice cultivars. Plant Physiol. Biochem. 57, 106113. Sharma, R.C., Duveiller, E., Ortiz-Ferrara, G., 2007. Progress and challenge towards reducing wheat spot blotch threat in the Eastern Gangetic Plains of South Asia: is climate change already taking its toll? Field Crop Res. 103, 109118. Singh, R., Singh, S., Parihar, P., Mishra, R.K., Tripathi, D.K., Singh, V.P., et al., 2016. Reactive oxygen species (ROS): beneficial companions of plants’ developmental processes. Front. Plant Sci. 7, 1299. Available from: https://doi.org/10.3389/fpls.2016.01299. Song, L., Ding, W., Zhao, M., Sun, B., Zhang, L., 2006. Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci. 171, 449458. Srivastava, S., Pathak, A.D., Gupta, P.S., Shrivastava, A.K., Srivastava, A.K., 2012. Hydrogen peroxide-scavenging enzymes impart tolerance to high temperature induced oxidative stress in sugarcane. J. Environ. Biol. 33, 657661. Sumesh, K.V., Sharma-Natu, P., Ghildiyal, M.C., 2008. Starch synthase activity and heat shock protein in relation to thermal tolerance of developing wheat grains. Biol. Plant. 52, 749753. Sun, C.W., Callis, J., 1997. Independent modulation of Arabidopsis thaliana polyubiquitin mRNAs in different organs of and in response to environmental changes. Plant J. 11, 10171027. Suzuki, N., Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Mittler, R., 2005. Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol. 139, 13131322. Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G., 2012. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35, 259270. Swindell, W.R., Huebner, M., Weber, A.P., 2007. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8, 125. Tahir, M.A., Aziz, T., Rahmatullah, 2011. Silicon induced growth and yield enhancement in two wheat genotypes differing in salinity tolerance. Commun. Soil Sci. Plant Anal. 42, 395407. Tan, W., Meng, Q.W., Brestic, M., Olsovska, K., Yang, X., 2011. Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. J. Plant Physiol. 168, 20632071. Tewari, R.K., Kumar, P., Tewari, N., Srivastava, S., Sharma, P.N., 2004. Macronutrient deficiencies and differential antioxidant responses-influence on the activity and expression of superoxide dismutase in maize. Plant Sci. 166, 687694. Tewari, R.K., Kumar, P., Sharma, P.N., 2006. Magnesium deficiency induced oxidative stress and antioxidant responses in mulberry plants. Sci. Hortic. 108, 714. Thines, B., Harmon, F.G., 2010. Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc. Natl. Acad. Sci. U.S.A. 107, 32573262. Thomashow, M.F., 1999. Plant cold acclimation, freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571599. Torok, Z., Goloubinoff, P., Horvath, I., Tsvetkova, N.M., Glatz, A., Balogh, G., et al., 2001. Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone mediated refolding. Proc. Natl. Acad. Sci. U.S.A. 98, 30983103. Uchida, A., Jagendorf, A., Hibino, T., Takabe, T., 2002. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 163, 515523. Valadabadi, S.A., Shiranirad, A.H., Farahani, H.A., 2010. Ecophysiological influences of zeolite and selenium on water deficit stress tolerance in different rapeseed cultivars. J. Ecol. Nat. Environ. 2, 154159. Valko, M., Morris, H., Cronin, M.T., 2005. Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 11611208. Van Doorn, W.G., Van Meeteren, U., 2003. Flower opening and closure: a review. J. Exp. Bot. 54, 18011812. Vierling, E., 1991. The role of heat shock proteins in plants. Annu. Rev. Plant Phys. 42, 579620.

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Further reading

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Vinocur, B., Altman, A., 2005. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr. Opin. Biotechnol. 16, 123132. Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R., 2007. Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199223. Wang, W., Vinocur, B., Shoseyov, O., Altman, A., 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244252. Wang, J.Z., Cui, L.J., Wang, Y., Li, J.L., 2009. Growth, lipid peroxidation and photosynthesis in two tall fescue cultivars differing in heat tolerance. Biol. Plant. 53, 237242. Waraich, E.A., Ahmad, R., Ashraf, M.Y., Saifullah, Ahmad, M., 2011. Improving agricultural water use efficiency by nutrient management in crop plants. Acta Agric. Scand. Sect. B: Plant Soil Sci. 61, 291304. Xu, S., Li, J., Zhang, X., Wei, H., Cui, L., 2006. Effects of heat acclimation pre treatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turf grass species under heat stress. Environ. Exp. Bot. 56, 274285. Xue, T., Hartikainen, H., Piironen, V., 2001. Antioxidative and growth-promoting effect of selenium on senescing lettuce. Plant Soil. 237, 5561. Yang, K.A., Lim, C.J., Hong, J.K., Park, C.Y., Cheong, Y.H., Chung, W.S., et al., 2006. Identification of cell wall genes modified by a permissive high temperature in Chinese cabbage. Plant Sci. 171, 175182. Yu, M., Lamattina, L., Spoel, S.H., Loake, G.J., 2014. Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol. 202, 11421156. Zhang, X., Cai, J., Wollenweber, B., Liu, F., Dai, T., Cao, W., et al., 2013. Multiple heat and drought events affect grain yield and accumulations of high molecular weight glutenin subunits and glutenin macropolymers in wheat. J. Cereal Sci. 57, 134140. Zhang, Y.Y., Wang, L.L., Liu, Y.L., Zhang, Q., Wei, Q.P., Zhang, W.H., 2006. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na1/H1 antiport in the tonoplast. Planta 224, 545555. Zhang, J.Z., Zhang, Q., Chen, Y.J., Sun, L.L., Song, L.Y., Peng, C.L., 2012. Improved tolerance toward low temperature in banana (Musa AAA group Cavendish Willimas). South Af. J. Bot. 78, 290294. Zinn, K.E., Tunc-Ozdemir, M., Harper, J.F., 2010. Temperature stress and plant sexual reproduction: uncovering the weakest links. J. Exp. Bot. 61, 19591968. Ziogas, V., Tanou, G., Filippou, P., Diamantidis, G., Vasilakakis, M., Fotopoulos, M., 2013. Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol. Biochem. 68, 118126. ´ ´ bek-Sokolnik, A., 2012. Temperature stress and responses of plants. In: Ahmad, P., Prasad, M.N.V. (Eds.), Zro Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Springer, New York, pp. 113134.

Further reading Ruelland, E., Zachowski, A., 2010. How plants sense temperature. Environ. Exp. Bot. 69, 225232.

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C H A P T E R

3 Salinity and its tolerance strategies in plants Muhammad Ashar Ayub1, Hamaad Raza Ahmad1, Mujahid Ali1, Muhammad Rizwan2, Shafaqat Ali2, Muhammad Zia ur Rehman1 and Aisha A. Waris1 1

Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan 2Department of Environmental Sciences & Engineering, Government College University Faisalabad, Faisalabad, Pakistan

3.1 Introduction Soil salinity is a major environmental issue of 21st century (Shrivastava and Kumar, 2015) especially in the arid and semiarid regions of the world (Mahmoodabadi et al., 2013; Wang et al., 2018). Of all the prevailing environmental issues including floods, high temperature, wind storms, and droughts, the most devastating one is soil salinity (Shahbaz and Ashraf, 2013; Shrivastava and Kumar, 2015). The term “soil salinization” reflects a combination of saline, sodic, and alkaline soils (Van Beek et al., 2010), which are characterized by high concentration of soluble salts, cations (Ca21, Na1, K1, and Mg21), carbonate 32 22 2 (CO22 3 ), bicarbonates (HCO ), sulfate (SO4 ), and nitrates (NO3 ) in the soil, respectively (Shrivastava and Kumar, 2015; Sha Valli Khan et al., 2014; Van Beek et al., 2010). According to Harmon and Daigh (2017), salinity and sodicity are abiotic stresses that can be simply defined as overabundance of soluble salts in soil. The excessive concentration of these salts in soil retards the production capacity of agricultural lands (Rehman et al., 2017) by affecting organic carbon mineralization and germination of crops (Kim et al., 2011; Nouri et al., 2017). The major anthropogenic factors behind this threat include the application of salinized water for irrigation (Di Gioia et al., 2018), and most importantly the land-use patterns (Wong et al., 2009; Harmon and Daigh, 2017). The natural factors are multiple that include low rainfall, high evaporation rate, poor cultural practices, and weathering of native rocks (Shrivastava and Kumar, 2015). Globally, these factors together

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3. Salinity and its tolerance strategies in plants

contribute to almost around 30% salt-affected lands (Jamil et al., 2011; Shrivastava and Kumar, 2015). Furthermore, the ratio of these lands is increasing at a rate of 10% each year and reached 50% value for overall arable lands under this stress in 2015 (Jamil et al., 2011).

3.1.1 Plants and salt stress Almost all crops show sensitivity to high salt levels (Liang et al., 2018), but it differs greatly between species and slightly among type of cultivar within a species (Di Gioia et al., 2018). The developmental growth stage of plant (Phogat et al., 2018) and the external environmental factors also alter plant response toward salinity (Di Gioia et al., 2018). Salt stress poses significant problem for agriculture systems by suppressing crop yield potential (Harmon and Daigh, 2017). The presence of excess salt concentration in soil not only effects the plants growth by reducing seed germination, plant height, root length, and fructification (Liang et al., 2014, 2018), but also it has indirect effects on section of food web that depends on that host plant (Harmon and Daigh, 2017). All this happens due to salt-induced oxidative stress (Horie et al., 2011), ion toxicity, and diminished photosynthesis rate in plants that ultimately result in significant decrease in overall crop yield (Rengasamy, 2010). Despite all this, plants naturally can survive and complete their life cycle in high salt stress conditions (Parida and Das, 2005). They have well-developed biological, chemical, and physiological mechanisms (Liang et al., 2018), which may lead to the formation of products and initiation of processes that improve plant tolerance against soluble salts (Parida and Das, 2005). These mechanisms could be of high complexity or low complexity depending on the types of changes they need to make in response to plant salt stress (Parida and Das, 2005). Several studies have revealed that sensing ability of plant stress and signaling machinery are the crucial components of their salt stress tolerance network (Deinlein et al., 2014). Among the plant internal chemical salt tolerance mechanisms, salt overly sensitive (SOS) signaling pathways (Zhang and Blumwald, 2001), hyperosmotic sensors (Deinlein et al., 2014), gene regulation in roots (Geng et al., 2013), plant membrane Na1 and K1 transporters (Schroeder et al., 2013) are the most popular ones (Deinlein et al., 2014). Moreover, osmoregulation and hormonal changes are biological salt tolerance adaptations of plants (Nahar et al., 2016; Khan and Khan, 2014). The plant growth-promoting rhizobacteria (PGPR) (Dodd and Perez-Alfocea, 2012), plant fungi association (Knappova´ et al., 2016), and application of organic and inorganic amendments (Miransari, 2014; Wang et al., 2017) are some other strategies that improve plant tolerance against salt stress. Scientists also adopted a promising physiological approach to mitigate this challenge in which they used salt tolerant engineered plants or transgenic saltresistant varieties (Deinlein et al., 2014). But, it was not very successful because the salt tolerance mechanism in plants is genetically very complex (Flowers, 2004; Liang et al., 2018).

3.2 Genesis and classification of saline soils 3.2.1 Genesis of saline soil Salt-affected soils refer to the presence of excessive soluble salts, sodium ions, and sometimes a combination of both of them (Qadir et al., 2007; Sastre-Conde et al., 2015).

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The process of salt-affected soil genesis is a slow, but continuous process (Rehman et al., 2017). The causes and sources of such soils are multiple and long studied since 19th century to explain their actual origin and formation (Hartemink and Bockheim, 2013). Generally, the nature of soil parent material, climatic features of a particular area, diversity of soil microorganisms, time, and topography/relief decide the nature and properties of saline soils (Simonson, 1995; Mansour and Salama, 2004). Over the course of years, it was found that persistent rise of salt deposits in salt-stressed soils is primarily due to physical and chemical weathering of organic and inorganic minerals of parent material that release primary minerals into the soil (Daliakopoulos et al., 2016; Nouri et al., 2017; Rehman et al., 2017). And the secondary sources include rainwater, seawater intrusions, wind-transported material, climate (especially low precipitation), human activities such as application of fertilizers, poor soil management, unjustifiable use of water, vegetation and land (Rengasamy, 2010; Nouri et al., 2017) and landscape features (physiographic unevenness) of an area (Rehman et al., 2017). In Pakistan, almost around 6.5 mha of land is salt affected (Qureshi et al., 2008), which mostly include saline sodic/sodic soils (Rehman et al., 2017). The country’s primary or ancient salt-stress concern is due to arid-to-semiarid climate, and the major secondary source is canal irrigation system (Rehman et al., 2017), which brings 16.6 million tons salts annually that sums up approximately 1 t salts per hectare per year in irrigated plains (Qureshi et al., 2008).

3.2.2 Sources of saline soils Plants confront salinity stress throughout their lives (Sha Valli Khan et al., 2014), especially in arid-to-semiarid regions due to low rainfall, presence of high salt-containing parent material and other geological and organic materials (Rengasamy, 2010; Rehman et al., 2017). Other natural factors include salt deposits from physiographic unevenness of a landscape, fossil salts, capillary rise of salty ground water, rainwater, wind-transported materials (Rengasamy, 2010), and marine water intrusions (Qureshi et al., 2008). The resultant buildup of salts from these sources causes primary salinization (Sha Valli Khan et al., 2014). In addition to this, anthropogenic contributing factors of salt stress include wastewater from various domestic, commercial, and urban effluents (Saha et al., 2014; Nouri et al., 2017), application of poor-quality irrigation water (Rehman et al., 2017), poor cultivation practices, use of soluble fertilizers (Rengasamy, 2010), and mismanagement of land and vegetation resources (Nouri et al., 2017). The discharge of salts from all these sources negatively influences soil ecosystem (Pilon-Smits, 2005; Nouri et al., 2017) and threatens the arable land productivity worldwide (Farooq et al, 2017).

3.2.3 Classification of saline soils Classification of saline soils is based upon the presence of soluble salts. The major groups include saline soils, sodic soils, and a combination of both (Brady and Weil, 2002). Around 40% salt-stressed soils of the world are saline in nature, and the

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TABLE 3.1 Soil salinity classes (Rasool et al., 2012; Wicke et al., 2011). Salinity class

EC (dS/m)

Nonsaline

0 2

Low saline

2 4

Moderately saline

4 8

Highly saline

8 16

Extremely saline

$ 16

remaining 60% are sodic in nature (Qadir et al., 2006; Nouri et al., 2017). Table 3.1 shows the classification of saline soils.

3.3 Effects of salinity and sodicity on soil physicochemical attributes Almost around 10% of lands under all climatic zones and 15% of cultivatable fields of the world have high salt contents in the soil slum or regolith (Munns and Tester, 2008; Sha Valli Khan et al., 2014). Soil affected by salinization and alkalization have the typical characteristics that include the accumulation of excess carbonates, sodium ions, and bicarbonates, high soil pH, high exchangeable sodium percentage (ESP), high sodium absorption ratio (SAR) at the soil surface (Qadir and Schubert, 2002). This higher/excess concentration results in the deterioration of chemical and physical properties of soil (Hogarth, 2015) to the degree of eliminating all vegetation (Trnka et al., 2013).

3.3.1 Effect on sodicity on soil physical and chemical properties Sodicity is characterized by high ESP or SAR of soil (Rengasamy, 2010) and accumulation of Na1 in relation to divalent cations (Ca21 and Mg21) (Cucci et al., 2013), which cause soil structure degradation and irreversible reduction in hydraulic conductivity (Rengasamy, 2010). Due to the dominance of sodium carbonate and the calcareous nature of these soils (Rengasamy, 2016), the availability of other ions is suppressed by decreasing their solubility, due to which different plant species develop deficiency symptoms (Briat et al., 2015). Moreover, sodicity greatly influences the physical properties of soil by affecting its structure through swelling, slaking, and dispersion of soil (Quirk, 2001), which contain swelling minerals (Cucci et al., 2013). This happens due to separation and expansion of soil clay particles by excess sodium ions interference (Nouri et al., 2017). During this process the dispersed particles block large soil pores and ultimately decrease their permeability (Mohanty et al., 2015), thus preventing normal water and air movement into and within soil (Nouri et al., 2017). As a consequence, soil structure destabilizes, there is limited infiltration of water into the soil, which leads to restricted availability of nutrients and moisture to plants (Chi and Wang, 2010; Rengasamy, 2016) and increased water logging, susceptibility to erosion and surface runoff (Warren et al., 2001; De la Paix et al., 2013).

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When soil dries out, sodic soils become dense, structure less, and clogged with small clay particles (Daliakopoulos et al., 2016) forming surface crusts and hard settings (Nouri et al., 2017), thus reducing hydraulic conductivity (Warren et al., 2001).

3.3.2 Effect on salinity on soil physical and chemical properties The aggregation and dispersion in soil depends on the presence of salinity and sodicity, or the combination of them. Unlike sodicity, salinization promotes soil aggregation process through flocculation of soil particles and thus improves the physical properties of soil (Hogarth, 2015). The presence of salt ions in soil, such as calcium and magnesium, boosts stabilization and aggregation properties through soil flocculation (Nouri et al., 2017). However, higher concentrations become problem for plants growing in saline soils and the soil itself by affecting its fertility (Hogarth, 2015) and physiochemical properties. First, the major soil salinity effect on soil chemical properties is sharp changes in pH and redox potential by complicating osmotic pressure and specific ion concentration of soil solution (Rengasamy, 2010). Due to high level of soluble salts and increased osmotic pressure, soil moisture level fluctuations become another major constraint of these soils (Rengasamy, 2006). As a result, there is reduced availability of water (Farooq et al., 2015) and imbalance in the uptake of nutrients by plants (Deinlein et al., 2014; Hogarth, 2015). Other than high osmotic pressure, adverse effects of increased electric conductivity (EC) of saline soils impact important soil processes, such as decomposition and respiration (Singh, 2015). Salinization of soil also effects some physical properties resulting in low permeability (Chi et al., 2012), rendering suppressed root growth, and therefore plant growth is hindered (Bui, 2017). As far as soil structure is concerned, saline soils do not affect it as sodic soils do when soluble salts leach down (Rengasamy, 2010). However, the buildup of salts with time starts deteriorating soil structure and hence hinders salt leaching (Rengasamy, 2006). Salinity also affects textural properties of soil as a result of which the plants cease to take up enough water and other compounds (Rengasamy, 2006; Rengasamy, 2010). All these physicochemical parameters act as major yield limiting factors in salt-affected soil and can be improved using phytoremediation and soil conditioning amendments (Miranda et al., 2018).

3.4 Effect of salinity on plant growth 3.4.1 Osmotic deregulations Glycophytes, the salinity-sensitive plants, strive to maintain their growth and development in salt-affected soils due to the hyperosmotic stress conditions (Tuteja, 2007). Salinity principally distresses plant physiology and metabolism through osmotic stress/ deregulation or water-deficit effects (Wang et al., 2003; Munns and Tester, 2008; Sha Valli Khan et al., 2014). Due to dissolved salt ions in soil solution adjacent to plant root cells, the difference in water and/or osmotic potential restricts plant ability to take up water, which leads toward “physiological drought” or “cellular dehydration” (Munns, 2005;

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Nouri et al., 2017). These detrimental effects ultimately stunt physiological growth of plants and reduce their annual yields (Parida and Das, 2005; Sha Valli Khan et al., 2014). In response to such an extreme condition of osmotic imbalance in soil, plants tend to transform their stomatal conductance to combat or withstand salinity stress (de Azevedo Neto et al., 2004). Seedling of Ziziphus mauritiana Lam. (Rhamnaceae) grown under different treatments of NaCl has shown reduced emergence and water potential and K1 ions act as competitor of Na1 ions (Bhatt et al., 2008). Most angiosperms are sensitive to salinity as their Na1/K1 ion channels are not fully functional thus opening an era of genetically engineered halotolerant plants to cope with osmotic stress (Cushman, 2001). Moreover, the hormonal and nutritional balance due to high salt contents in soil solution (El Sayed, 2011) restricts growth of all grain legumes (Murillo-Amador et al., 2007).

3.4.2 Specific ion toxicity Higher soil concentration of mineral nutrients creates hyperionic condition that disrupts plant homeostatic control that results in ionic stress and/or toxicity (Deinlein et al., 2014; Sha Valli Khan et al., 2014). This condition disturbs normal metabolic processes in plants causing stunted growth and development (Tuteja, 2007; White and Brown, 2010; Jogaiah et al., 2012). Under saline conditions, plants face sodium ions toxicity due to their high solubility (Bhatt et al., 2008). Nutritional imbalance due to accumulation of Na1 and Cl2 ions enter cellular compartments through transpiration stream starts causing oxidative, nutritional, and mechanical stresses in plants (Deinlein et al., 2014; Sha Valli Khan et al., 2014). Crop plants adopt different anatomical modifications to cope with such condition (AcostaMotos et al., 2017). This high concentration of Na1 starts competition with K1 influx that ultimately alters K1/Na1 ratio (Tuteja, 2007). This condition results in Na1 toxicity, osmotic imbalance, disrupted stomatal functioning, and activity of some enzymes (Tuteja, 2007). Moreover, Na1 ion toxicity also adversely affects soil physical and chemical properties (Qadir and Schubert, 2002), which have bearing on plant water uptake, root penetration, seedling emergence, and ultimately the plant growth and yield (Hogarth, 2015). In addition to Na1, the presence of Cl2 also negatively influences plant growth (Farooq et al., 2017). Another negative outcome of ion toxicity is the gradual death of older leaves (Munns et al., 2006), and ultimately their senescence takes place in plants due to uptake of excess amount of salt ions (Sehrawat et al., 2013). To sense and cope with the detrimental effects of ion toxicity, plants have multiple physiological, mechanical, chemical, and biological mechanisms (Munns, 2005; Khan and Khan, 2014). Several research findings report the presence of specific genes (Hakeem et al., 2012), production of metabolites and proteins in plants for salt ion toxicity (Kosova´ et al., 2013).

3.5 Plant responses to salinity 3.5.1 Physiological adaptation To cope with salinity stress, plants must adopt different physiological modification explained in the following sections.

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3.5.1.1 Stomatal conductance and photosynthetic activity Plant physiological adaptation to salinity stress is a complex phenomenon (Stepien and Johnson, 2008). Photosynthesis, being the primary target of salt stress in plants, is a biochemical process that is directly inhibited by the presence of salts (Ste˛pien´ and Kłbus, 2006; Abdul Qados, 2011), especially due to sodium chloride (Stepien and Johnson, 2008). First, high level of salts interferes with plant water uptake that plants encounter by stopping stomatal conductance. Consequently, plant does not get enough CO2 through stomata and thus stops its photosynthetic activity (Stepien and Johnson, 2008). These changes result in huge plant growth and productivity losses (Sudhir and Murthy, 2004) because plants develop oxidative stress whereby reactive oxygen species (ROS) form in chloroplast, which damage protein, structural membranes, and genetic material of plants (Asada, 2000). Results of certain studies confirm the negative impact of salinity on photosynthetic pigment (chlorophyll) formation (Sudhir and Murthy, 2004; Taffouo et al., 2010; Kapoor and Srivastava, 2010) and decrease total carotenoid contents (Parida and Das, 2005). Moreover, ion toxicity and salinity stress effects growth, leaf area, and stomatal conductance of plants as well (Brugnoli and Lauteri, 1991). Some other studies also show that salinity stress adversely affects stomatal conductance and photosynthetic activity of many plants such as Rhizophora mangle, also known as red mangrove (Biber, 2006). To fight salt stress the primary focus of plant is to regain normal water potential. In order to increase plant water use efficiency, plants, such as Mesembryanthemum crystallinum and Atriplex lentiformis, shift from C3 mode to C4 or crassulacean acid metabolism (CAM) that allow them to control transpiration losses of water and withstand prolonged salinity (Parida and Das, 2005). Some plants such as sugar beet have tendency to maintain stomatal conductance to nullify salinity impacts (Katerji et al., 1997), which can be used to screen osmotic and salinity-tolerant plant varieties (Rahnama et al., 2010). It is observed that plants, such as barley, have increased in situ concentration of ABA that rapidly increases in photosynthetic tissues in response to high NaCl concentration to stabilize the stomatal conductance of plant that was disturbed by high salt contents (Fricke et al., 2006; Munns and Tester, 2008). With salt stress plant leaves develop a large number of small stomata in plants, for example, Fusarium oxysporum f. sp. melonis (Solmaz et al., 2011). In the presence of Na1 ions, plants accumulate Ca21 ions in guard cells, which tend to reduce the closing response of Na1 ions (Perera et al., 1995). C3 plants might face diffusive and metabolic limitations in C assimilation (photosynthesis) in saline conditions (Flexas et al., 2004) and decrease pigments necessary for photosynthesis (Abdul Qados, 2011). While some plant in salinity stress produces hormones to reduce impact of salinity on carbon metabolism (Omoto et al., 2012). Membrane transports such as SOS1, AtHKT1, and AtNHX1 and Na1 pups help plant to withstand stress in Arabidopsis (Zhang and Shi, 2013). Better plant nutrient acquisition reduces detrimental photosynthetic pigment decrease due to salt stress (Shah et al., 2017). Halotolerant plants have several mechanisms to carry out proper physiological mechanisms in saline environment (Wungrampha et al., 2018). Salt stress induces the production of amicicides such as proline and plant hormones, which help to reduce ROS activities and plant uptake water to conduct photosynthetic activities (Rady et al., 2016; Tabot and Adams, 2014).

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3.5.2 Biochemical adaptation 3.5.2.1 Osmotic regulations Osmotic stress directly affects plant growth and development due to the presence of high salt concentration ( . 40 mM NaCl) in the vicinity of roots (Munns and Tester, 2008). Inorganic ions, such as Na1, K1, Ca21, and Cl2, play an important role in osmotic adjustments under saline-derived osmotic stress as their excessive uptake disturbs ions homeostatic in whole plant system (Parida and Das, 2005). In saline stress, plant experiences serious osmotic stress and bring anatomical changes to counter it by maintaining tissue osmotic potential (Chen and Jiang, 2010). Both halophytes and glycophytes either restrict extra salt entry into their vacuoles or send them to different tissues for their proper metabolism (Zhu, 2003). Mostly older plant tissues are used for salt storage compartmentalization, which are ultimately lost when the salts contents cross a certain level (Cheeseman, 1988; Parida and Das, 2005). Moreover, the enzymes such as vacuolar type H1-ATPase and the vacuolar pyrophosphatase are also used by plants for salt removal, especially sodium (Dietz et al., 2001). This strategy is mainly used by halophyte plants to get rid of excess salt from plant cytoplasm (de Lourdes Oliveira Otoch et al., 2001; Wang et al., 2001). In addition to this, different osmolytes and osmoprotectants are also produced by plants to serve this purpose (Nahar et al., 2016). All these adjustments are made by plants for regulating water contents or osmoregulation (Deinlein et al., 2014). 3.5.2.2 Oxidative modification Salinity stress experienced by plants triggers the production of many ROS and reactive nitrogen species (RNS), which can damage plants (Ben Rejeb et al., 2014; Turkan, 2018), but plant have the capability to adopt regulatory mechanism and exclusion strategies to control these toxins (Møller et al., 2007). Mainly plants try to detoxify plants from these species by releasing certain enzymes, such as superoxide dismutase, ascorbate peroxidase, catalase, and the various peroxidases for ROS regulation (Logan, 2007; Foyer and Noctor, 2005). By releasing these enzymes, plant manages to create equilibrium between the production and removal of ROS species to protect plant photosystems from photoinhibition and reverse changes in photosynthesis induced by salt stress (Apel and Hirt, 2004; Munns and Tester, 2008). After this, plant adopts other adjustments, such as changes in leaf morphology and alterations is plant biochemical processes that prevent the damage of these toxins (Munns and Tester, 2008). Other than all these adjustments, oxidative modification in response to salinity stress is also conducted by changing cytosolic composition of ions and pH (Kader and Lindberg, 2010). Researches have shown that some plant bodies under shock develops configurational modification in stress proteins and amino acids (Jacques et al., 2013), which could be driven by plant nutrition such as sulfur (Nazar et al., 2011) and silicon (Coskun et al., 2016). 3.5.2.3 Intercellular signaling Plant response to salt stress does not take more than a second (Tracy et al., 2008). Initially, plant responds to salinity stress by triggering plant shoots that receive signals by ABA production in the roots. This signaling is important for roots to adjust their functions to cope with elevated sodium concentration as well as to allow shoots to alter their

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functioning (Munns and Tester, 2008; Tracy et al., 2008). Moreover, it is believed that plasma membrane proteins are considered first signal sites of this danger, so that plant changes its internal environment (Munns and Tester, 2008). Another pathway characterized as one of the best intercellular salt stress signaling pathways in plants is the elevated level of cytosolic calcium ions that are sensed by calcineurin B-like proteins (Zhu, 2002). The activation of the membrane-bound Na1/H1 antiporter with senores and transducers (Padan et al., 2001) also plays an important role in developing salinity tolerance in plants by immediately responding to high ion concentration in the environment (Møller and Tester, 2007). In addition to all these, cell starts behaving like an entity and tries to counter stress by many other different cellular mechanisms and adaptations as well, such as configurational changes in plasma membrane and protoplast viscosity (Mansour and Salama, 2004). Plant cells also have mechanism of core cellular pathways to deal with salinity stress. Major signaling pathways are energy-based sensing, and signaling triggers changes in stress proteins necessary for osmotic balance, water transport, and metabolic gene expressions (Zhu, 2001, 2002, 2003). This is how plants respond to changes in extracellular salt concentration by changing its various functional aspects (Sunkar and Zhu, 2007; Yamaguchi-Shinozaki and Shinozaki, 2006). 3.5.2.4 Hormone regulation Growth hormones if applied exogenously act as phytoprotectants under salinity and sodicity stresses. 3.5.2.4.1 Hormonal-modified proline metabolism and plant growth

Proline is low-molecular-weight amino acid, which is a part of many proteins in plant body (Lehmann et al., 2010) and can also accumulate in plant as solute (Per et al., 2017) to help plant tolerate salt stress (Iqbal et al., 2014; Khan and Khan, 2014). Proline helps plant to ameliorate oxidative stress initiated by environmental stresses such as soil salinity by maintaining photosynthetic activity and lowering plant tissue water potential, which help plant uptake water from soil (Rady et al., 2016; Tabot and Adams, 2014). Saline stress is responsible for the generation of ROS as stress signal in plants, proline metabolism thus is an important key edge for plant to tolerate salinity stress (Ibria et al., 2017; Ben Rejeb et al., 2014). ROS produced in saline stress can damage biomolecules (lipids, protein, and amino acids) in plants, and proline saves plant from these effects as it controls redox potential of cell and energy balance (Giberti et al., 2014). Proline biosynthesis in plants is initiated by an enzyme Δ1-pyrroline-5-carboxylate synthetase (P5C5) that requires ATP and nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) (Hu et al., 1992). Its level in different plant parts varies, and its production is controlled by different stimuli such as light, metabolites, and hormones (Lehmann et al., 2010). Nitrogen being part of proline plays a key role in proline metabolism (Khan et al., 2015), and with N and S application, plant leaf proline contents increase (Rais et al., 2013). Similarly, Ca is also important for proline metabolism (Parre et al., 2007). Plant hormones have direct and indirect impact on proline contents as they can control nutrient acquisition (Kiba et al., 2010). A detailed review of proline metabolism under action of plant hormones is discussed in the following sections.

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3.5.2.4.1.1 Abscisic acid ABA is 15 carbon sesquiterpenoid (C15H20O4) plant hormone produced under stress conditions and controls many plant growth and development responses as well as the production of proline in cells (Finkelstein, 2013). ABA metabolism in plants involves feedback mechanism under action of environmental stresses such as drought and salinity and circannual rhythms (Seung et al., 2011). In Arabidopsis, ABA controls carbohydrate metabolism by triggering initial two steps (Kempa et al., 2008). Plant under salinity, drought, and heavy metal stress modifies ABA biosynthesis by activating different ABA-responsive genes (Vishwakarma et al., 2017). Makela et al. (2003) proposed that plant ABA induces proline production under stress. Arabidopsis P5CS1 activity is controlled by ABA under water and salinity stress (Strizhov et al., 1997; Verslues and Bray, 2005). Barley leaves socked in 20 ppm solution of ABA help plant produce proline at rate of 1 μmole/h/g dry weight. Basic mechanism behind this was initiation of proline synthesis by glutamic acid pathway controlled by ABA (Stewart, 1980). Exogenous application of ABA also increases proline contents of Eucalyptus camaldulensis shoot grown in vitro, but salt-tolerant clone shows more production of proline under salinity stress than salt sensitive (Woodward and Bennett, 2005). Under saline condition and other abiotic stress, ABA controls a large variety of proteomes being produced in plant tissue and helping it maintain tissue homeostasis (Woodward and Bennett, 2005). 3.5.2.4.1.2 Ethylene Ethylene, a gaseous hormone produced in plants under salinity stress (Groen and Whiteman, 2014; Khan and Khan, 2014), helps plant in acclimation of stress involving hydrogen peroxide signaling pathway (Zhu et al ., 2016). Proline and ethylene are involved in salt tolerance in plants, and their metabolism is controlled by N fertilization in mustard (Iqbal et al., 2015) and also under action of other growth regulators such as salicylic acid (SA) (Khan et al., 2013). Lutts et al. (1996) have reported that higher saline stress higher will be ethylene production in rice leaves. Environmental factors such as light intensity and duration affect ethylene metabolism in plants (Rodrigues et al., 2014). Salt stress can increase proline and polyamine concentration in tissue of Helianthus annuus (Alvarez et al., 2003). A research conducted by Zapata et al. (2017) shows that salinity stress given to different plants can increase its ethylene and proline concentration while polyamine concentration decreases. 3.5.2.4.1.3 Salicylic acid Salicylic is involved in increasing proline metabolism under salinity stress (Iqbal et al., 2014; Fayez and Bazaid, 2014) and exogenous application of SA helps plant mitigate salinity stress (Jini and Joseph, 2017). Proline helps plant to tolerate salinity stress (Kahlaoui et al., 2018) and SA can improve proline metabolism as reported by Misra and Saxena (2009) for lentil plants. SA can improve growth and photosynthetic activity of Hordeum vulgare (Pancheva et al., 1996), lentils (Misra and Saxena, 2009), marigold (Pacheco et al., 2013), and mustard (Nazar et al., 2015). SA application along with Ca improved growth, physiological parameters, and activity of antioxidant enzymes, which help in salinity tolerance in Triticum aestivum L. (Al-Whaibi et al., 2011). SA application improved morphological characteristics of Aloe vera grown under salinity stress (Miri et al., 2014), and 300 μM SA proved statistically significant impact on plant growth parameters and proline contents of cowpea (Afshari et al., 2013).

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3.5.2.4.1.4 Nitric oxide Nitric oxide (NO) is a gaseous ROS produced under abiotic and biotic stress signaling pathways (Domingos et al., 2015) and disease defense system pathway (Delledonne et al., 1998). Plants product NO under salinity stress to initiate the production of compounds involved in salinity stress mitigation (Gomes et al., 2017). Nitric oxide has a significant role in proline metabolism modification under salinity. Sodium nitroprusside (SNP) is a donor of NO and when applied exogenously in concentration 100 μM under sodic stress showed significant improvement in proline contents of cucumber seedlings (Fan et al., 2012). About 0.05 mM SNP and 0.05 mM SA applied to Gossypium hirsutum L. under salinity stress showed protective effect against salinity stress. They helped plant lower lipid peroxidation, detoxification of ROS and improve ion uptake and balance and activate metabolism of osmotic-regulated substances (Dong et al., 2015). Study conducted by Bai et al. (2011) has shown that NO has protective role of proteomic and physiological level for maize plant under salinity stress. Moreover, it also enhanced antioxidant enzyme activity and controlled H2O2 production. NO has shown to improve tomato fruit quality by enhancing health-promoting biomolecules (Ali and Ismail, 2014).

3.5.3 Cellular mechanisms 3.5.3.1 Na1 exclusion from the cell Upon interaction of plants with sodic environment it tends to absorb Na1 through roots. Na1 along with water takes the simplest pathway and involves different ion channels to move into the cell where it regulates osmotic balance and causes toxicity in excess amount (Zhang et al., 2010). It is very important therefore to exclude or restate Na entry into cell. Arabidopsis plant is reported to have different cyclic nucleotide signaling pathways that control voltage-gated Na channels and thus act as a check (Maathuis and Sanders, 2001). Besides cyclic nucleotides, Ca21, ROS generation also play a role in Na1 uptake control (Maathuis et al., 2014). Upon Na1 toxicity plant modifies Na uptake at root soil interface. Plant cells tend to increase Ca concentration inside their cytoplasm. An increase in (Ca21) can be detected by the CBL (SOS3/CBL4) proteins. Activation of SOS3/ CBL4 is followed by protein interaction with the serine/threonine protein kinase SOS2/ CIPK24 (Halfter et al., 2000). The SOS3/CBL4 SOS2/CIPK24 complex migrates to the plasma membrane Na1/H1 antiporter SOS1 and increases its activity by phosphorylating the C-terminus of the SOS1 protein (Zhu, 2001). Arabidopsis cells can produce a protein called Qc-SNARE under the action of gene AtSFT12, which can sequester Na1 in vacuoles if plants make it nontoxic for cell (Tarte et al., 2015). 3.5.3.2 Na1 transporters To mitigate Na1 toxicity, a number of Na transporters are working in cell membranes of plants, and ion transporter plays an important role in ion balance in plants (Hasegawa, 2013). HKT1;4 in rice are reported to be involved in Na exclusion from leaf blades (Suzuki et al., 2016). In mutant rice varieties, t-DNA controls the activity of OsHKT1;4 that enforce Na exclusion form leaf tissues (Oda et al., 2018). Halophytes are involved salt excretion glands that can excrete 30 mmol/m2/day salts in mangroves (Sua´rez and Medina, 2008). Moreover, plant transporters and channels such as

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H1-ATPases, SOS1, HKTs, and NHXs help plant in Na exclusion (Almeida et al., 2017; Keisham et al., 2018). The Na1/H1 antiporter present in tonoplast (NHX1) and on plasma membrane (SOS1) was found in Arabidopsis and later controlled by SOS2 and SOS3 that are Ca21-activated complex (Serrano and Rodriguez-Navarro, 2001). Major Na transporters in Arabidopsis are AtSOS1, AtNHX, and AtHKT1;1 involved in Na toxicity tolerance (Horie et al., 2009). To eliminate toxicity of Na1, plant cell accumulates it in their vacuoles or other subcellular parts. In this regard, Na1/H1 antiporter plays an important role. H1-ATPase creates a proton gradient and energizes its efflux into apoplast or influx to vacuoles for compartmentation (Hasegawa, 2013).

3.5.4 Tissue tolerance to ions 3.5.4.1 Solute accumulation in cells Osmotic adjustment in plant cell is considered to have a key role in salinity tolerance strategies. Plants need to cope with external higher salt concentration by maintaining higher solutes in their cell. The greatest portion of ionic intake takes place through the epidermal cells of plant root hairs (Apse and Blumwald, 2007). Unlike the normal physiological condition of plants, salt stress results in passive Na1 influx into the cytosol through ion channels, such as HKT, LCT1, and NSCC (Garciadebla´s et al., 2003; Horie and Schroeder, 2004; Apse and Blumwald, 2007). Yin et al. (2010) used C-13 labeling and reported that Solanum lycopersicum plant upon experiencing salinity stress that produces huge amounts of carbohydrates solutes in its cells under the influence of AgpL1 and AgpS1. Plant grown under salinity can change their tissue solute concentration diurnally and seasonally (Sa´nchez-Blanco et al., 1998) and can modify their cellular solutes under influence of triggered gene expression under salinity (Yin et al., 2010). Plant facing salinity stress if comes under symbiotic association with fungi can also trigger accumulation of oxalic acid while under no symbiotic plant succinic acid is predominant in plant tissues (Sheng et al., 2010). Plant cell solute accumulation is a well-tested useful approach for osmotic balance under salinity (Benzarti et al., 2014). 3.5.4.1.1 Compartmentation of Na1 inside cell

A diversity of taxonomic variation in plants allows them to sustain Na toxicity in saltaffected soils by sequestering them into their vacuoles. This compartmentation of Na1 ions into the vacuole protects the cytosol from its harmful effects (Apse and Blumwald, 2007). This transport is completely controlled by cation/H1 antiporters (Bassil and Blumwald, 2014). In addition to these transporters, NHX-like protein transporters also have demonstrated their regulatory functions when plant is growing under high salt conditions (Apse and Blumwald, 2007). Several studies conducted on wheat and cotton crops have proven the utility of cation/H1 antiporters and NHX-like protein transporters utility in improving salt tolerance in plants (Wu et al., 2004; Saqib et al., 2005). In a wide variety of transgenic plant species, compartmentation of sodium ions by these transporters has ameliorated the toxic effects on plant metabolism (Yamaguchi and Blumwald, 2005).

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3.5.4.1.2 Homeostasis

Plan cell tends to balance its cellular somatic conditions to cope with hypertonic or hypotonic environment. Salt stress tolerant faces Na1 toxicity as it is being uptaken in plants along with other solutes. Na being toxic to plant needs to be moved out of cells of compartmentalized in the cell to eliminate its toxicity. Radial transportation of Na in plant tissues and its sequestration in vacuole is the best option for Na homeostasis under salt stress (Apse and Blumwald, 2007). Sodium ion mimics action of K in cell and can disturb physiological functions of plant. K1/Na1 homeostasis plays an important role in maintaining Na concentration in the cell (Almeida et al., 2017). Ethylene-mediated Na/K homeostasis in plants under saline stress is also very well-known phenomenon (Jiang et al., 2013). 3.5.4.1.3 Apoplastic alkalization and reacidulation

Apoplastic pH is a variable that tends to be changing under salinity stress. Under the influence of Cl2 ions, plant leaf apoplast gets alkanized due to the activation of Cl2/2H1 symporters moving H1 and Cl2 into cell (Geilfus, 2017). Under NaCl stress, activity of HATPase activity has been reported to be upregulated in halophyte plant like M. crystallinum L. (Barkla et al., 1995). Cell membranes and tonoplast have a huge number of H1/ Na1 antiporters, which transfer Na into vacuole and H1 in apoplast and controlled by ABA-dependent signaling pathway (Barkla et al., 1999; Geilfus, 2017; Silva et al., 2009). NaCl stress can induce alkalinity in apoplast of plant tissues (Geilfus and Mu¨hling, 2012). Under saline stress Cl2-mediated alkalinity can be reversed by the action of plasma membrane H-ATPase working in antiport with Na influx. When cation concentration increases in apoplast PM-H1-ATPase activates and pour H into apoplast. This is necessary to provide charge balancing in apoplast (Geilfus, 2017). Vascular Na1/H1 NHX-type antiporters are also responsible for K homeostasis in plant cell as it is being affected by Na or other cations (McCubbin et al., 2014).

3.6 Microbe plant interaction Plant microbe interaction is a very long-studied concept. Plant growth-promoting bacteria are classified into four groups: rhizospheric (sticking to roots or present in rhizosphere), enophytic (residing inside plant), symbiotic (involved in biological nitrogen fixation (BNF) and lives in nodules) and phyllospheric (sticking on leaves/stem) (Glick, 2014). PGPR when inoculated with plant seed perform very efficiently in helping plant surpass period of salt stress (Dodd and Perez-Alfocea, 2012) and drought (Vurukonda et al., 2016).

3.6.1 Plant growth-promoting rhizobacteria Soil salinity is widespread problem, and we can ameliorate stress in plant by isolation rhizosphere salt-tolerant PGPR. These microbes have a wide mechanism of beneficial interaction with plant experiencing abiotic and biotic stresses (Dodd and Perez-Alfocea, 2012).

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Exogenous application of PGPR in saline and nonsaline conditions is possible, and their population can not only survive in such conditions but also help plant withstand stress. PGPR strains were found to be effective in controlling of foot and root rot of tomato under saline conditions and also enhancing plant stress tolerance capacity by modifying ROS balance and proline contents in tomato (Egamberdieva et al., 2017). Exogenous application of PGPR helps rice withstanding salinity, improving growth, nutrient acquisition, and antioxidant production (Jha and Subramanian, 2013). Under stress condition, plant ethylene levels become high, a microbe called 1aminocyclopropane-1-carboxylate (ACC) deaminase producing microbe can contribute to lower down plant ethylene concentration, thus helping plant withstand abiotic stress such as saline stress (Glick, 2014). These ACC deaminase producing PGPR have been isolated from rhizosphere and help plant if applied exogenously withstand environmental stress (Bal et al., 2012). Halotolerant Enterobacter species is reported to displace ACC-deaminase activity and promote rice seedling growth under saline conditions (Sarkar et al., 2018). PGPR are involved in the production of plant growth stimulants in rhizosphere and help plant in sequestering more nutrients, upregulation of plant hormones and suppressing pathogenic and/or abiotic stresses. PGPR if applied, both under normal or stress conditions, promote plant growth and suppress plant stresses via production of biocontrol agents (Ahemad and Kibret, 2014). 3.6.1.1 Hormone production for enhanced growth PGPR trigger the production of plant hormones in plant, which can help plant withstand salinity stress (Numan et al., 2018). PGPR when come in contact with stressed plant produce ACC deaminase, osmolytes, antioxidants, and other exogenous secretions such as exopolysaccharides, phytohormones, and volatile compounds (Vurukonda et al., 2016). The role of PGPR in the production of these plant growth stabilizers is of great importance for sustainable saline agriculture (Gouda et al., 2018). PGPR involved in the production of indole acetic acid (IAA) help plant enhance growth (Damam et al., 2016). Moreover PGPR strains are also involved in the production of other phytohormones such as IAA (Damam et al., 2016; Cassa´n et al., 2013), cytokinins (Liu et al., 2013; de Garcia Salamone et al., 2005; Cassa´n et al., 2013), gibberellins (Kang et al., 2014; Cassa´n et al., 2013; Ryu et al., 2005), and Ryu et al. (2005) have also reported that phytohormones produced by PGPR help plant withstand saline stress experience by plants. The PGPR and its metabolites can be isolated from plant rhizosphere and if inoculate exogenously can help plant with stand abiotic stress.

3.6.2 Halotolerant microbe mediated processes Halophytes are organisms, which can live, grow, and multiply in extreme saline conditions. Genomic make up of halotolerant microbes make them capable of tolerating high salinity stress (Etesami and Beattie, 2018). Halotolerant microbes can tolerate very high salt stress that exceed beyond capability of any other living organism. Out of many possible way of salinity stress tolerance, three are well known: passive homeostasis of solutes in cytoplasm, contrasting cytoplasm to make compatible osmotic balance with

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environment, and third one is changes in cell physiology to resist cell plasmolysis and withstand harsh osmotic stress (Gupta and Huang, 2014). Nonhalophyte crops are facing extreme stress in saline conditions. Halotolerant bacteria from rhizosphere of these crops can be mined and after their possible inoculation in soil with proper population they act as halophilic PGPR involved in stress mitigation of plants (Etesami and Beattie, 2018). Halotolerant PGPR have been reported in mitigating salinity stress in wheat (Orhan, 2016), peanut (Sharma et al., 2016; Shukla et al., 2011), okra (Habib et al., 2016), and sugarbeat (Zhou et al., 2017). Basic mechanism of halotolerant microbes and plant interaction is similar to other PGPR. They improve plant osmotic balance, nutrient acquisition, Ca1 metabolism, and phytohormone-mediated stress mitigation (Shukla et al., 2011). They are also involved in the production of ROS scavenger enzymes helpful in lowering oxidative stress to plants (Habib et al., 2016). Plant PGPR interaction is a helpful tool for saline agriculture if applied with proper knowledge.

3.6.3 Fungal plant interaction Among soil microbes, fungi have a distinctive identity and importance. Plant fungi association popularly known as mychorrhizae has significant role in plant nutrient acquisition, stress mitigation, biomolecules detoxification, and phytohormones production. About 90% of plant species have these associations balancing plant nutritionnutrition, and environmental stress promotes the healthy growth of mycorrhizal association (Garcia and Mendoza, 2008). 3.6.3.1 Arbuscular mycorrhizae in salt-affected soils Arbuscular mycorrhizae (AM) are asexual, obligate, and symbiotic fungi with exclusive morphological and genomic construction allowing it to colonize soil and roots of plants. AM are characterized by external fungal growth on roots. AM have high tendency to grow in moderate or extreme salinity conditions (Knappova´ et al., 2016) and help plant withstand salinity by various mechanisms. AM help plant in balanced nutrient acquisition balancing Na:K in tissue, increasing root surface area, bring biochemical, physiological, and molecular modification in plants under salinity stress (Evelin et al., 2009). Besides improving nutritional aspects of plant AM association also improves production of biomolecules (proline, phytohormones, enzymes to detoxify ROS) in plant (Porcel et al., 2011). AM-associated plans have shown better water balance, improved photosynthesis and fruit quality under water stress condition (Asrar and Elhindi, 2011), which is also an effect of salinity. 3.6.3.2 Impact of arbuscular mycorrhizae plant association on plant growth AM association in S. lycopersicum L. is reported to mitigate salinity stress by the upregulation of nutrient acquisition, net assimilation rate, higher activity of ROS scavenger enzymes compared to noninoculated plants (Hajiboland et al., 2009) and improves agronomic growth of wheat (Tofighi et al., 2017). AM wheat association helps wheat improve nutrient acquisition, accumulation of soluble sugars, photosynthesis, and ion balance

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under elevated salinity and CO2 stress (Zhu et al., 2016), and decreases Na1 uptake (Mardukhi et al., 2011). Among all species of AM Glomus etunicatum is the right species for wheat crop to get economical production under saline condition (Daei et al., 2009). In bajara cultivar, AM inoculation enhances antioxidant activity and proline accumulation under salinity stress compared to noninoculated plants (Borde et al., 2011). Study conducted by Estrada et al. (2013) shows that isolated AM form salinity hit area and perform better in suppressing salinity stress on maize crop when applied exogenously.

3.7 Effect of different amendments in tolerance against salinity Organic and inorganic amendments can improve soil structure and specific ion toxicity in severely salt-affected soils. Organic and inorganic amendments can eliminate Na from exchange system and help reclaim sodic, saline sodic soils as well as provide plants with balances nutrition (Walker and Bernal, 2008; Eghball et al., 1999; Eichler-Lo¨bermann et al., 2007). Addition of these amendments such as biochar (Blanco-Canqui, 2017; Saifullah et al., 2018), farm yard manure (Diacono and Montemurro, 2015), and gypsum (Rasouli et al., 2013) can improve soil physical properties for better reclamation of saline soils (Tejada et al., 2006).

3.7.1 Organic amendments Organic amendments help reclaim salt-affected soil ore affectively and also support growth of crops in these soils (Larney and Angers, 2012; Tejada et al., 2006). Among these notable ones are animal and crop manure (Himmelstein et al., 2014;Tejada et al., 2009), processed composts (Bastida et al., 2015;Tavarini et al., 2011), and biochar, which are very important for recovering soil physicochemical properties and soil health (Scotti et al., 2015). Organic amendments support growth, reproduction, and decomposition activity of microbes in saline soils (Chahal et al., 2017), which help in phytohormone secretion and mitigation of salinity stress to plants (Miransari, 2014). Biochar, a famous organic amendment, has proven to be effective against NaCldeveloped salinity stress in soil grown with potato corp. It increases ABA concentration in leaves and lowering Na1/K1 ration of plant shoot (Patel et al., 2017). Application of biochar increases soil AM and helps mitigate salinity stress (Hammer et al., 2015) and maintain population of soil biota (Lehmann et al., 2011). Exogenously applied biochar not only helps plant withstand salinity but also improves its growth, yield, and physiology (Akhtar et al., 2015). Animal manure another important organic amendments are necessary to build up soil carbon stock in organic matter deprived soils (Maillard and Angers, 2013) and improve agronomic parameters of plants (Cha-um and Kirdmanee, 2011; Shaaban et al., 2013). Compost made from different plant sources is another carbon source for soil and helpful in managing good soil physicochemical properties of soil (Mylavarapu and Zinati, 2009). Industrial waste compost and vermicompost applied on maize crop were proven to be effective in mitigating salinity stress and improving maize production compared to control (Oo et al., 2013). For low-input agriculture system, compost is very

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important soil amendment for obtaining maximum economic yield (Oue´draogo et al., 2001). Biochar and compost both are helpful in mitigating salinity stress by improving Na leaching and supporting plant growth (Chaganti et al., 2015).

3.7.2 Inorganic amendments Inorganic soil amendments are also helpful in managing saline agriculture such as gypsum (Raza et al., 2001; Ilyas et al., 1997), modified gypsum (Wang et al., 2017), rock phosphate (Husnain et al., 2014), and lime (Inagaki et al., 2016). Saline sandy loam soil when applied with gypsum showed improved physicochemical properties (Valzano et al., 1997). Saline soils act as precursor of saline sodic and sodic soils if not treated properly (Rehman et al., 2017). Saline sodic and sodic soils can be reclaimed using gypsum as a source of Ca for the replacement of Na from exchange sites (Giovanna et al., 2012). Gypsum amendments can help get sustainable crop yield even when crop is being fed with high solute (Na1) irrigation water in rice wheat cropping system (Bajwa and Josan, 1989) modified gypsum such as flue-gas desulfurization (simplified as FGD) gypsum is successfully used in china over more than 120 sq km for reclamation of saline sodic soils, this gypsum is safe in term of heavy metal pollutants and can enhance soil capacity to sequester organic carbon (Wang et al., 2017). Rock phosphate amended compost has shown to be more effective in providing available phosphorus in alkaline soils compared to only compost application (Yadav et al., 2017). Just like other inorganic amendments combined application of lime and gypsum with no till practice can not only enhance soil productivity and soil fertility (Inagaki et al., 2016) but also significantly improve soil physicochemical properties such as soil EC, SAR, exchangeable Na, and saline soil infiltration rate (Makoi and Verplancke, 2010) required for better reclamation.

3.8 Genetic modification in plants to enhance tolerance against salinity In nature, some plants have evolved genetic modifications to withstand salinity tolerance and using modern-day genetic engineering and biotechnology we can insert stress suppressing gene/genes into other plants to make them salt tolerant (Roy et al., 2014). Some genes in plants have been over expressed to help plant withstand salinity such as Na transporter gene in wheat (Munns et al., 2012). HKT-mediated ion exclusion as explained earlier is also a well-defined and explained phenomenon in monocots and Arabidopsis (Horie et al., 2009). Ion exclusion, tissue tolerance, and stress signaling are under control of genes in halotolerant plants, which can be transported to normal plants to make them salt tolerant (Roy et al., 2014).

3.9 Genetic engineering of halotolerant plants Biotechnology, genetic engineering, and conventional breeding are being used to create salt tolerance in crop plants. Genetic engineering and biotechnology has helped to

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introduce genes for osmoprotectants and ion transporters in salt-sensitive plant to improve their halotolerance (Ashraf and Akram, 2009). Genetic biotechnology involves several ways to induce/trigger specific gene or mutate already present one (Papdi et al., 2010). Ethyl methanesulfonate (EMS) mutagenesis of plants is a well-tested approach, which can induce point mutation in DNA of plants altering gene expression and help screen out favorable phenotypic expression (Weigel and Glazebrook, 2006). If gene of interest has to be inserted in host plant cell/callus then T-DNA insertion mutagenesis can be used. Introduction of ion transporters and ion channels in plants such as Na1/H1 aniporter Atriplex gmelini in rice reported to have increased salt tolerance in crop (Ohta et al., 2002). This modification in rice genome can increase rice indiginious salt tolerance capacity which previously was merely due to ion exclusion and osmotic tolerance (Munns and Tester, 2008). Besides ion transporters and channels, transcription factors and various signaling pathways are also important in salinity tolerance, and genetically engineered plants can have these characteristics (Turan et al., 2018).

3.10 Summary The presence of high salt concentration is an abiotic stress to which almost all agricultural crops are sensitive (Liang et al., 2018). Under salt stress, plant instantly faces osmotic stress that affects plant growth and development (Liang et al., 2014). After osmotic stress, plants experience ionic toxicity when the salt level reaches a threshold level due to which plant loses its homeostasis (Munns and Tester, 2008). Finally, a series of secondary stresses that lead to oxidative stress (Ibria et al., 2017), disturbance in photosynthetic activity (Abdul Qados, 2011), stomach conductance, and osmotic regulations (Munns et al., 2006) and result in prominent decrease in plant growth, development, and overall productivity (Rengasamy, 2010). The growth of plant roots, shoots, and height has drastically reduced (Liang et al., 2018). Such events led to the scientific investigation of salt stress in plants with the aim to control it and protect the plants (Zhu, 2001). Plants develop many physiological, biological, and chemical adjustments in response to salt stress (Pastori, 2002). These include accumulation of osmotic adjustment substances, ion-specific absorption, compartmentalization, scavenging of ROS, and research of salt tolerance genes (Liang et al., 2018). This is how plants respond to the ion, osmotic and oxidative stresses under salt stress. Detailed study of all these mechanisms provides the theoretical basis to understand plant adjustments against salts and how we can further enhance plant salt tolerance. Ultimately, this will help in increasing the quality and yield of crops in salty lands. At present, transgenic technology is the most feasible and attractive option to help develop plants that can fight salt stress (Liang et al., 2018).

References Abdul Qados, A.M.S., 2011. Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). J. Saudi Soc. Agric. Sci. 10, 7 15. Acosta-Motos, J., Ortun˜o, M., Bernal-Vicente, A., Diaz-Vivancos, P., Sanchez-Blanco, M., Hernandez, J., 2017. Plant responses to salt stress: adaptive mechanisms. Agronomy 7, 18.

Plant Life under Changing Environment

References

65

Afshari, M., Shekari, F., Azimkhani, R., Habibi, H., Fotokian, M.H., 2013. Effects of foliar application of salicylic acid on growth and physiological attributes of cowpea under water stress conditions. Iran Agric. Res 32, 55 70. Agrawal, R., Gupta, S., Gupta, N.K., Khandelwal, S.K., Bhargava, R., 2013. Effect of sodium chloride on gas exchange, antioxidative defense mechanism and ion accumulation in different cultivars of Indian jujube (Ziziphus mauritiana L.). Photosynthetica 51, 95 101. Ahemad, M., Kibret, M., 2014. Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J. King Saud Univ. Sci. 26, 1 20. Akhtar, S.S., Andersen, M.N., Liu, F., 2015. Residual effects of biochar on improving growth, physiology and yield of wheat under salt stress. Agric. Water Manage. 158, 61 68. Ali, H.E.M., Ismail, G.S.M., 2014. Tomato fruit quality as influenced by salinity and nitric oxide. Turk. J. Bot. 38, 122 129. Almeida, D.M., Oliveira, M.M., Saibo, N.J.M., 2017. Regulation of Na1 and K1 homeostasis in plants: towards improved salt stress tolerance in crop plants. Genet. Mol. Biol. 40, 326 345. Alvarez, I., Tomaro, M.L., Benavides, M.P., 2003. Changes in polyamines, proline and ethylene in sunflower calluses treated with NaCl. Plant Cell Tiss Org culture 74 (2003), 51 59. Al-Whaibi, M.H., Siddiqui, M.H., Basalah, M.O., 2011. Salicylic acid and calcium-induced protection of wheat against salinity. Protoplasma 249, 769 778. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373 399. Apse, M.P., Blumwald, E., 2007. Na1 transport in plants. FEBS Lett. 581, 2247 2254. Asada, K., 2000. The water-water cycle as alternative photon and electron sinks. Philos. Trans. R. Soc., B: Biol. Sci. 355, 1419 1431. Ashraf, M., Akram, N.A., 2009. Improving salinity tolerance of plants through conventional breeding and genetic engineering: an analytical comparison. Biotechnol. Adv. 27, 744 752. Asrar, A.W.A., Elhindi, K.M., 2011. Alleviation of drought stress of marigold (Tagetes erecta) plants by using arbuscular mycorrhizal fungi. Saudi J. Biol. Sci. 18, 93 98. de Azevedo Neto, A.D., Prisco, J.T., Ene´as-Filho, J., de Lacerda, C.F., Silva, J.V., Costa, P.H.A., et al., 2004. Effects of salt stress on plant growth, stomatal response and solute accumulation of different maize genotypes. Braz. J. Plant Physiol. 16, 31 38. Bai, X., Yang, L., Yang, Y., Ahmad, P., Yang, Y., Hu, X., 2011. Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. J. Proteome Res. 10, 4349 4364. Bajwa, M.S., Josan, A.S., 1989. Effect of gypsum and sodic irrigation water on soil and crop yields in a rice—wheat rotation. Agric. Water Manage. 16, 53 61. Bal, H.B., Nayak, L., Das, S., Adhya, T.K., 2012. Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil 366, 93 105. Barkla, B.J., Zingarelli, L., Blumwald, E., Smith, J.A.C., 1995. Tonoplast Na1/H1 antiport activity and its energization by the vacuolar H1-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiol. 109, 549 556. Barkla, B.J., Vera-Estrella, R., Maldonado-Gama, M., Pantoja, O., 1999. Abscisic acid induction of vacuolar H1ATPase activity in Mesembryanthemum crystallinum is developmentally regulated. Plant Physiol. 120, 811 820. Bassil, E., Blumwald, E., 2014. The ins and outs of intracellular ion homeostasis: NHX-type cation/H1 transporters. Curr. Opin. Plant Biol. 22, 1 6. Bastida, F., Selevsek, N., Torres, I.F., Herna´ndez, T., Garcı´a, C., 2015. Soil restoration with organic amendments: linking cellular functionality and ecosystem processes. Sci. Rep. 5, 15550. Ben Rejeb, K., Abdelly, C., Savoure´, A., 2014. How reactive oxygen species and proline face stress together. Plant Physiol. Biochem. 80, 278 284. Benzarti, M., Rejeb, K.B., Messedi, D., Mna, A.B., Hessini, K., Ksontini, M., et al., 2014. Effect of high salinity on Atriplex portulacoides: growth, leaf water relations and solute accumulation in relation with osmotic adjustment. S. Afr. J. Bot. 95, 70 77. Bhatt, M.J., Patel, A.D., Bhatti, P.M., Pandey, A.N., 2008. Effect of soil salinity on growth, water status and nutrient accumulation in seedlings of Ziziphus mauritiana (Rhamnaceae). J. Fruit Ornament. Plant Res 16, 383 401. Biber, P.D., 2006. Measuring the effects of salinity stress in the red mangrove, Rhizophora mangle L. Afr. J. Agric. Res 1, 1.4.

Plant Life under Changing Environment

66

3. Salinity and its tolerance strategies in plants

Blanco-Canqui, H., 2017. Biochar and soil physical properties. Soil Sci. Soc. Am. J. 84, 687. Borde, M., Dudhane, M., Jite, P., 2011. Growth photosynthetic activity and antioxidant responses of mycorrhizal and non-mycorrhizal bajra (Pennisetum glaucum) crop under salinity stress condition. Crop Prot. 30, 265 271. Brady, N., Weil, R., 2002. The Nature and Properties of Soils, 13th ed Prentice Hall, Upper Saddle River, NJ. Briat, J.F., Dubos, C., Gaymard, F., 2015. Iron nutrition, biomass production, and plant product quality. Trends Plant Sci. 20, 33 40. Brugnoli, E., Lauteri, M., 1991. Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L.) and Salt-Sensitive (Phaseolus vulgaris L.) C(3) non-halophytes. Plant Physiol. 95, 628 635. Bui, E.N., 2017. Causes of Soil Salinization, Sodification, and Alkalinization. Oxford University Press. Cassa´n, F., Vanderleyden, J., Spaepen, S., 2013. Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. J. Plant Growth Regul. 33, 440 459. ˇ unek, ˚ Chaganti, V.N., Crohn, D.M., Sim J., 2015. Leaching and reclamation of a biochar and compost amended saline-sodic soil with moderate SAR reclaimed water. Agric. Water Manage. 158, 255 265. Chahal, S.S., Choudhary, O.P., Mavi, M.S., 2017. Organic amendments decomposability influences microbial activity in saline soils. Arch. Agron. Soil Sci. 63, 1875 1888. Cha-um, S., Kirdmanee, C., 2011. Remediation of salt-affected soil by the addition of organic matter: an investigation into improving glutinous rice productivity. Sci. Agric. 68, 406 410. Cheeseman, J.M., 1988. Mechanisms of salinity tolerance in plants. Plant Physiol. 87, 547 550. Chen, H., Jiang, J.-G., 2010. Osmotic adjustment and plant adaptation to environmental changes related to drought and salinity. Environ. Rev. 18, 309 319. Chi, C.M., Wang, Z.C., 2010. Characterizing salt-affected soils of Songnen Plain using saturated paste and 1:5 soilto-water extraction methods. Arid L. Res. Manage. 24, 1 11. Chi, C.M., Zhao, C.W., Sun, X.J., Wang, Z.C., 2012. Reclamation of saline-sodic soil properties and improvement of rice (Oriza sativa L.) growth and yield using desulfurized gypsum in the west of Songnen Plain, northeast China. Geoderma 187 188, 24 30. Coskun, D., Britto, D.T., Huynh, W.Q., Kronzucker, H.J., 2016. The role of silicon in higher plants under salinity and drought stress. Front. Plant Sci. 7, 1072. Cucci, G., Lacolla, G., Rubino, P., 2013. Irrigation with saline-sodic water: effects on soil chemical-physical properties. Afr. J. Agric. Res. 8, 358 365. Cushman, J.C., 2001. Osmoregulation in plants: implications for agriculture. Am. Zool. 41, 758 769. Daei, G., Ardekani, M.R., Rejali, F., Teimuri, S., Miransari, M., 2009. Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J. Plant Physiol. 166, 617 625. Daliakopoulos, I.N., Tsanis, I.K., Koutroulis, A., Kourgialas, N.N., Varouchakis, A.E., Karatzas, G.P., et al., 2016. The threat of soil salinity: a European scale review. Sci. Total Environ. 573, 727 739. Damam, M., Moinuddin, M.K., Kausar, R., 2016. Isolation and screening of plant growth promoting actinomycetes from rhizosphere of some forest medicinal plants. Int. J. Chem. Tech. Res 9, 521 528. de Garcia Salamone, I.E., Hynes, R.K., Nelson, L.M., 2005. Role of cytokinins in plant growth promotion by rhizosphere bacteria. PGPR Biocontrol Biofert, 173 195. De la Paix, M.J., Lanhai, L., Xi, C., Ahmed, S., Varenyam, A., 2013. Soil degradation and altered flood risk as a consequence of deforestation. L. Degrad, Dev 24, 478 485. de Lourdes Oliveira Otoch, M., Menezes Sobreira, A.C., Farias de Araga˜o, M.E., Orellano, E.G., da Guia Silva Lima, M., Fernandes de Melo, D., 2001. Salt modulation of vacuolar H1-ATPase and H1-pyrophosphatase activities in Vigna unguiculata. J. Plant Physiol. 158, 545 551. Deinlein, U., Stephan, A.B., Horie, T., Luo, W., Xu, G., Schroeder, J.I., 2014. Plant salt-tolerance mechanisms. Trends Plant Sci. 19, 371 379. Delledonne, M., Xia, Y., Dixon, R.A., Lamb, C., 1998. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585 588. Diacono, M., Montemurro, F., 2015. Effectiveness of organic wastes as fertilizers and amendments in salt-affected soils. Agriculture 5, 221 230.

Plant Life under Changing Environment

References

67

Di Gioia, F., Rosskopf, E.N., Leonardi, C., Giuffrida, F., 2018. Effects of application timing of saline irrigation water on broccoli production and quality. Agric. Water Manage. 203, 97 104. Dietz, K.J., Tavakoli, N., Kluge, C., Mimura, T., Sharma, S.S., Harris, G.C., et al., 2001. Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J. Exp. Bot. 52, 1969 1980. Dodd, I.C., Perez-Alfocea, F., 2012. Microbial amelioration of crop salinity stress. J. Exp. Bot. 63, 3415 3428. Domingos, P., Prado, A.M., Wong, A., Gehring, C., Feijo, J.A., 2015. Nitric oxide: a multitasked signaling gas in plants. Mol. Plant 8, 506 520. Dong, Y.J., Wang, Z.L., Zhang, J.W., Liu, S., He, Z.L., He, M.R., 2015. Interaction effects of nitric oxide and salicylic acid in alleviating salt stress of Gossypium hirsutum L. J. Soil Sci. Plant Nutr. 15, 561 573. Egamberdieva, D., Davranov, K., Wirth, S., Hashem, A., Abd_Allah, E.F., 2017. Impact of soil salinity on the plant-growth—promoting and biological control abilities of root associated bacteria. Saudi J. Biol. Sci. 24, 1601 1608. Eghball, B., Wienhold, B.J., Gilley, J.E., 1999. Managing manure phosphorus. In: Proc. Integr. Crop Manag. Conf. Eichler-Lo¨bermann, B., Ko¨hne, S., Koppen, D., 2007. Effect of organic, inorganic, and combined organic and inorganic P fertilization on plant P uptake and soil P pools. J. Plant Nutr. Soil Sci. 170, 623 628. El Sayed, H.E.S.A., 2011. Influence of salinity stress on growth parameters, photosynthetic activity and cytological studies of Zea mays L., plant using hydrogel polymer. Agric Biol J N. Am 2, 907 920. Estrada, B., Aroca, R., Maathuis, F.J.M., Barea, J.M., Ruiz-Lozano, J.M., 2013. Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant Cell Environ. 36, 1771 1782. Etesami, H., Beattie, G.A., 2018. Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front. Microbiol. 9, 148. Evelin, H., Kapoor, R., Giri, B., 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann. Bot. 104, 1263 1280. Fan, H.F., Du, C.X., Guo, S.R., 2012. Effect of nitric oxide on proline metabolism in cucumber seedlings under salinity stress. J. Am. Soc. Hortic. Sci 137, 127 133. Farooq, M., Hussain, M., Wakeel, A., Siddique, K.H.M., 2015. Salt stress in maize: effects, resistance mechanisms, and management. A review. Agron. Sustain. Dev. 35, 461 481. Farooq, M., Gogoi, N., Hussain, M., Barthakur, S., Paul, S., Bharadwaj, N., et al., 2017. Effects, tolerance mechanisms and management of salt stress in grain legumes. Plant Physiol. Biochem. 118, 199 217. Fayez, K.A., Bazaid, S.A., 2014. Improving drought and salinity tolerance in barley by application of salicylic acid and potassium nitrate. J. Saudi Soc. Agric. Sci. 13, 45 55. Finkelstein, R., 2013. Abscisic acid synthesis and response. Arabidopsis Book 11, e0166. Flexas, J., Bota, J., Loreto, F., Cornic, G., Sharkey, T.D., 2004. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol. 6, 269 279. Flowers, T.J., 2004. Improving crop salt tolerance. J. Exp. Bot. 55, 307 319. Foyer, C.H., Noctor, G., 2005. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28, 1056 1071. Fricke, W., Akhiyarova, G., Wei, W., Alexandersson, E., Miller, A., Kjellbom, P.O., et al., 2006. The short-term growth response to salt of the developing barley leaf. J. Exp. Bot. 57, 1079 1095. Garcia, I.V., Mendoza, R.E., 2008. Relationships among soil properties, plant nutrition and arbuscular mycorrhizal fungi plant symbioses in a temperate grassland along hydrologic, saline and sodic gradients. FEMS Microbiol. Ecol. 63, 359 371. Garciadebla´s, B., Senn, M.E., Ban˜uelos, M.A., Rodrı´guez-Navarro, A., 2003. Sodium transport and HKT transporters: the rice model. Plant J. 34, 788 801. Geilfus, C.-M., 2017. The pH of the apoplast: dynamic factor with functional impact under stress. Mol. Plant 10, 1371 1386. Geilfus, C.-M., Mu¨hling, K.-H., 2012. Ratiometric monitoring of transient apoplastic alkalinizations in the leaf apoplast of living Vicia faba plants: chloride primes and PM-H1-ATPase shapes NaCl-induced systemic alkalinizations. New Phytol. 197, 1117 1129. Geng, Y., Wu, R., Wee, C.W., Xie, F., Wei, X., Chan, P.M.Y., et al., 2013. A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25, 2132 2154.

Plant Life under Changing Environment

68

3. Salinity and its tolerance strategies in plants

Giberti, S., Funck, D., Forlani, G., 2014. Δ1-pyrroline-5-carboxylate reductase from Arabidopsis thaliana: stimulation or inhibition by chloride ions and feedback regulation by proline depend on whether NADPH or NADH acts as co-substrate. New Phytol. 202, 911 919. Giovanna, C., Giovanni, L., Mauro, P., Rocco, L., 2012. Reclamation of saline and saline-sodic soils using gypsum and leaching water. Afr. J. Agric. Res. 7, 6508 6514. Glick, B.R., 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169, 30 39. Gomes, M.A.C., Pestana, I.A., Santa-Catarina, C., Hauser-Davis, R.A., Suzuki, M.S., 2017. Salinity effects on photosynthetic pigments, proline, biomass and nitric oxide in Salvinia auriculata aubl. Acta Limnol. Bras. 29, 1 13. Gouda, S., Kerry, R.G., Das, G., Paramithiotis, S., Shin, H.-S., Patra, J.K., 2018. Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol. Res. 206, 131 140. Groen, S.C., Whiteman, N.K., 2014. The evolution of ethylene signaling in plant chemical ecology. J. Chem. Ecol. 40, 700 716. Gupta, B., Huang, B., 2014. Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int. J. Genomics 1 20. Habib, S.H., Kausar, H., Saud, H.M., 2016. Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed. Res. Int. 2016, 6284547. Hajiboland, R., Aliasgharzadeh, N., Laiegh, S.F., Poschenrieder, C., 2009. Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331, 313 327. Hakeem, K.R., Khan, F., Chandna, R., Siddiqui, T.O., Iqbal, M., 2012. Genotypic variability among soybean genotypes under NaCl stress and proteome analysis of salt-tolerant genotype. Appl. Biochem. Biotechnol. 168, 2309 2329. Halfter, U., Ishitani, M., Zhu, J.K., 2000. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. U.S.A. 97, 3735 3740. Hammer, E.C., Forstreuter, M., Rillig, M.C., Kohler, J., 2015. Biochar increases arbuscular mycorrhizal plant growth enhancement and ameliorates salinity stress. Appl. Soil Ecol. 96, 114 121. Harmon, J.P., Daigh, A.L.M., 2017. Attempting to predict the plant-mediated trophic effects of soil salinity: a mechanistic approach to supplementing insufficient information. Food Webs 13, 67 79. Hartemink, A.E., Bockheim, J.G., 2013. Soil genesis and classification. Catena 104, 251 256. Hasegawa, P.M., 2013. Sodium (Na1) homeostasis and salt tolerance of plants. Environ. Exp. Bot. 92, 19 31. Himmelstein, J.C., Maul, J.E., Everts, K.L., 2014. Impact of five cover crop green manures and Actinovate on Fusarium wilt of watermelon. Plant Dis. 98, 965 972. Hogarth, P.J., 2015. Mangroves and seagrasses. Biology of Mangroves Seagrasses. Oxford University Press, 198 207. Horie, T., Hauser, F., Schroeder, J.I., 2009. HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci. 14, 660 668. Horie, T., Kaneko, T., Sugimoto, G., Sasano, S., Panda, S.K., Shibasaka, M., et al., 2011. Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots. Plant Cell Physiol. 52, 663 675. Horie, T., Schroeder, J.I., 2004. Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol 136, 2457 2462. Hu, C.A., Delauney, A.J., Verma, D.P., 1992. A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc. Natl. Acad. Sci 89, 9354 9358. Husnain, Rochayati, S., Sutriadi, T., Nassir, A., Sarwani, M., 2014. Improvement of soil fertility and crop production through direct application of phosphate rock on Maize in Indonesia. Procedia Eng. 83, 336 343. Ilyas, M., Qureshi, R.H., Qadir, M.A., 1997. Chemical changes in a saline-sodic soil after gypsum application and cropping. Soil Technol. 10, 247 260. Inagaki, T.M., de Moraes Sa´, J.C., Caires, E.F., Gonc¸alves, D.R.P., 2016. Lime and gypsum application increases biological activity, carbon pools, and agronomic productivity in highly weathered soil. Agric. Ecosyst. Environ. 231, 156 165. Iqbal, N., Umar, S., Khan, N.A., Khan, M.I.R., 2014. A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ. Exp. Bot. 100, 34 42. Iqbal, N., Umar, S., Khan, N.A., 2015. Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J. Plant Physiol. 178, 84 91.

Plant Life under Changing Environment

References

69

Jacques, S., Ghesquie`re, B., Van Breusegem, F., Gevaert, K., 2013. Plant proteins under oxidative attack. Proteomics 13, 932 940. Jamil, A., Riaz, S., Ashraf, M., Foolad, M.R., 2011. Gene expression profiling of plants under salt stress. CRC. Crit. Rev. Plant Sci. 30, 435 458. Jha, Y., Subramanian, R., 2013. Paddy plants inoculated with PGPR show better growth physiology and nutrient content under saline conditions. Chil. J. Agric. Res. 73, 213 219. Jiang, C., Belfield, E.J., Cao, Y., Smith, J.A.C., Harberd, N.P., 2013. An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 25, 3535 3552. Jini, D., Joseph, B., 2017. Physiological mechanism of salicylic acid for alleviation of salt stress in rice. Rice Sci. 24, 97 108. Jogaiah, S., Govind, S.R., Tran, L.-S.P., 2012. Systems biology-based approaches toward understanding drought tolerance in food crops. Crit. Rev. Biotechnol. 33, 23 39. Kader, M.A., Lindberg, S., 2010. Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal. Behav. 5, 223 238. Kahlaoui, B., Hachicha, M., Misle, E., Fidalgo, F., Teixeira, J., 2018. Physiological and biochemical responses to the exogenous application of proline of tomato plants irrigated with saline water. J. Saudi Soc. Agric. Sci. 17, 17 23. Kang, S.M., Khan, A.L., You, Y.H., Kim, J.G., Kamran, M., Lee, I.J., 2014. Gibberellin production by newly isolated strain Leifsonia soli SE134 and its potential to promote plant growth. J. Microbiol. Biotechnol. 24, 106 112. Kapoor, K., Srivastava, A., 2010. Assessment of salinity tolerance of Vigna mungo Var. Pu-19 using ex vitro and in vitro methods. Asian J. Biotechnol. 2, 73 85. Katerji, N., Hoorn, J.V., Hamdy, A., 1997. Osmotic adjustment of sugar beets in response to soil salinity and its influence on stomatal conductance, growth and yield. Agric. Water, 57 69. Keisham, M., Mukherjee, S., Bhatla, S., 2018. Mechanisms of sodium transport in plants—progresses and challenges. Int. J. Mol. Sci. 19, 647. Kempa, S., Krasensky, J., Dal Santo, S., Kopka, J., Jonak, C., 2008. A central role of abscisic acid in stress-regulated carbohydrate metabolism. PLoS One 3, e3935. Khan, N.A., Khan, M.I.R., 2014. The ethylene: from senescence hormone to key player in plant metabolism. J Plant Biochem. Physiol 2, e124. Khan, M.I.R., Iqbal, N., Masood, A., Per, T.S., Khan, N.A., 2013. Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal. Behav. 8, e26374. Khan, M.I.R., Trivellini, A., Fatma, M., Masood, A., Francini, A., 2015. Role of ethylene in responses of plants to nitrogen availability. Front. Plant Sci. 6, 927. Kiba, T., Kudo, T., Kojima, M., Sakakibara, H., 2010. Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J. Exp. Bot. 62, 1399 1409. Kim, S., Rayburn, A.L., Voigt, T., Parrish, A., Lee, D.K., 2011. Salinity effects on germination and plant growth of prairie cordgrass and switchgrass. Bioenergy Res. 5, 225 235. Knappova´, J., Pa´nkova´, H., Mu¨nzbergova´, Z., 2016. Roles of arbuscular mycorrhizal fungi and soil abiotic conditions in the establishment of a dry grassland community. PLoS One 11, e0158925. Kosova´, K., Pra´sˇ il, I., Vı´ta´mva´s, P., 2013. Protein contribution to plant salinity response and tolerance acquisition. Int. J. Mol. Sci. 14, 6757 6789. Larney, F.J., Angers, D.A., 2012. The role of organic amendments in soil reclamation: a review. Can. J. Soil Sci. 92, 19 38. Lehmann, S., Funck, D., Szabados, L., Rentsch, D., 2010. Proline metabolism and transport in plant development. Amino Acids 39, 949 962. Lehmann, J., Rillig, M.C., Thies, J., Masiello, C.A., Hockaday, W.C., Crowley, D., 2011. Biochar effects on soil biota—a review. Soil Biol. Biochem. 43, 1812 1836. Liang, W., Cui, W., Ma, X., Wang, G., Huang, Z., 2014. Function of wheat Ta-UnP gene in enhancing salt tolerance in transgenic Arabidopsis and rice. Biochem. Biophys. Res. Commun. 450, 794 801. Liang, W., Ma, X., Wan, P., Liu, L., 2018. Plant salt-tolerance mechanism: a review. Biochem. Biophys. Res. Commun. 495, 286 291. Liu, F., Xing, S., Ma, H., Du, Z., Ma, B., 2013. Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl. Microbiol. Biotechnol. 97, 9155 9164.

Plant Life under Changing Environment

70

3. Salinity and its tolerance strategies in plants

Logan, B.A., 2007. Reactive oxygen species and photosynthesis. Antioxidants and Reactive Oxygen Species in Plants. Blackwell Publishing Ltd. Lutts, S., Kinet, J.M., Bouharmont, J., 1996. Ethylene production by leaves of rice (Oryza sativa L.) in relation to salinity tolerance and exogenous putrescine application. Plant Sci. 116, 15 25. Maathuis, F.J., Sanders, D., 2001. Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiol. 127, 1617 1625. Maathuis, F.J.M., Ahmad, I., Patishtan, J., 2014. Regulation of Na1 fluxes in plants. Front. Plant Sci. 5, 467. Mahmoodabadi, M., Yazdanpanah, N., Sinobas, L.R., Pazira, E., Neshat, A., 2013. Reclamation of calcareous saline sodic soil with different amendments (I): redistribution of soluble cations within the soil profile. Agric. Water Manage. 120, 30 38. Maillard, E´., Angers, D.A., 2013. Animal manure application and soil organic carbon stocks: a meta-analysis. Global Change Biol. 20, 666 679. Makela, P., Munns, R., Colmer, T.D., Peltonen-Sainio, P., 2003. Growth of tomato and an ABA-deficient mutant (sitiens) under saline conditions. Physiol. Plant. 117, 58 63. Makoi, J.H., Verplancke, H., 2010. Effect of gypsum placement on the physical chemical properties of a saline sandy loam soil. Aust. J. Crop Sci 4, 556. Mansour, M.M.F., Salama, K.H.A., 2004. Cellular basis of salinity tolerance in plants. Environ. Exp. Bot. 52, 113 122. Mardukhi, B., Rejali, F., Daei, G., Ardakani, M.R., Malakouti, M.J., Miransari, M., 2011. Arbuscular mycorrhizas enhance nutrient uptake in different wheat genotypes at high salinity levels under field and greenhouse conditions. Comptes Rendus Biol. 334, 564 571. McCubbin, T., Bassil, E., Zhang, S., Blumwald, E., 2014. Vacuolar Na1/H1 NHX-type antiporters are required for cellular K1 homeostasis, microtubule organization and directional root growth. Plants 3, 409 426. Miranda, M.F.A., dos Santos Freire, M.B.G., Almeida, B.G., Freire, A.G., Freire, F.J., Pessoa, L.G.M., 2018. Improvement of degraded physical attributes of a saline-sodic soil as influenced by phytoremediation and soil conditioners. Arch. Agron. Soil Sci. 64, 1207 1221. Miri, N., Nejad, F.M., Zeinali, H., 2014. Effect of salicylic acid and salinity on some morphological characteristics of Aloe vera. Am.-Eurasian J. Agric. Environ. Sci 14, 660 663. Miransari, M., 2014. Use of Microbes for the Alleviation of Soil Stresses, Vol. 1. Berlin: Springer. Misra, N., Saxena, P., 2009. Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci. 177, 181 189. Mohanty, S.K., Saiers, J.E., Ryan, J.N., 2015. Colloid mobilization in a fractured soil during dry wet cycles: role of drying duration and flow path permeability. Environ. Sci. Technol. 49, 9100 9106. Møller, I.S., Tester, M., 2007. Salinity tolerance of Arabidopsis: a good model for cereals? Trends Plant Sci. 12, 534 540. Møller, I.M., Jensen, P.E., Hansson, A., 2007. Oxidative modifications to cellular components in plants. Annu. Rev. Plant Biol. 58, 459 481. Munns, R., 2005. Genes and salt tolerance: bringing them together. New Phytol. 167, 645 663. Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651 681. Munns, R., James, R.A., La¨uchli, A., 2006. Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57, 1025 1043. Munns, R., James, R.A., Xu, B., Athman, A., Conn, S.J., Jordans, C., et al., 2012. Wheat grain yield on saline soils is improved by an ancestral Na1 transporter gene. Nat. Biotechnol. 30, 360 364. ´ vila-Serrano, N., Garcı´a-Herna´ndez, J.L., Murillo-Amador, B., Yamada, S., Yamaguchi, T., Rueda-Puente, E., A et al., 2007. Influence of calcium silicate on growth, physiological parameters and mineral nutrition in two legume species under salt stress. J. Agron. Crop Sci. 193, 413 421. Mylavarapu, R.S., Zinati, G.M., 2009. Improvement of soil properties using compost for optimum parsley production in sandy soils. Sci. Hortic. (Amsterdam) 120, 426 430. Nahar, K., Hasanuzzaman, M., Fujita, M., 2016. Roles of osmolytes in plant adaptation to drought and salinity. Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies. Springer, New Delhi. Nazar, R., Iqbal, N., Masood, A., Syeed, S., Khan, N.A., 2011. Understanding the significance of sulfur in improving salinity tolerance in plants. Environ. Exp. Bot. 70, 80 87.

Plant Life under Changing Environment

References

71

Nazar, R., Umar, S., Khan, N.A., Sareer, O., 2015. Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. S. Afr. J. Bot. 98, 84 94. Nouri, H., Chavoshi Borujeni, S., Nirola, R., Hassanli, A., Beecham, S., Alaghmand, S., et al., 2017. Application of green remediation on soil salinity treatment: a review on halophytoremediation. Process Saf. Environ. Prot. 107, 94 107. Numan, M., Bashir, S., Khan, Y., Mumtaz, R., Shinwari, Z.K., Khan, A.L., et al., 2018. Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review. Microbiol. Res. 209, 21 32. Oda, Y., Kobayashi, N., Tanoi, K., Ma, J., Itou, Y., Katsuhara, M., et al., 2018. T-DNA tagging-based gain-offunction of OsHKT1;4 reinforces Na exclusion from leaves and stems but triggers Na toxicity in roots of rice under salt stress. Int. J. Mol. Sci. 19, 235. Ohta, M., Hayashi, Y., Nakashima, A., Hamada, A., Tanaka, A., Nakamura, T., et al., 2002. Introduction of a Na1/ H1 antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett. 532, 279 282. Omoto, E., Taniguchi, M., Miyake, H., 2012. Adaptation responses in C4 photosynthesis of maize under salinity. J. Plant Physiol. 169, 469 477. Oo, A.N., Iwai, C.B., Saenjan, P., 2013. Soil properties and maize growth in saline and nonsaline soils using cassavaindustrial waste compost and vermicompost with or without earthworms. L. Degrad. Dev. 26, 300 310. Orhan, F., 2016. Alleviation of salt stress by halotolerant and halophilic plant growth-promoting bacteria in wheat (Triticum aestivum). Braz. J. Microbiol. 47, 621 627. Oue´draogo, E., Mando, A., Zombre´, N.P., 2001. Use of compost to improve soil properties and crop productivity under low input agricultural system in West Africa. Agric. Ecosyst. Environ. 84, 259 266. Pacheco, A.C., Cabral, C., Fermino, E.S.S., Aleman, C.C., 2013. Salicylic acid-induced changes to growth, flowering and flavonoids production in marigold plants. J. Med. Plants Res 1, 95 100. Padan, E., Venturi, M., Gerchman, Y., Dover, N., 2001. Na 1 /H 1 antiporters. Biochim. Biophys. Acta Bioenerg. 1505, 144 157. Pancheva, T.V., Popova, L.P., Uzunova, A.N., 1996. Effects of salicylic acid on growth and photosynthesis in barley plants. J. Plant Physiol. 149, 57 63. Papdi, C., Leung, J., Joseph, M.P., Salamo, I.P., Szabados, L., 2010. Genetic screens to identify plant stress genes. Plant Stress Tolerance. Humana Press, pp. 282 291. Parida, A.K., Das, A.B., 2005. Salt tolerance and salinity effects on plants: a review. Ecotoxicol. Environ. Saf. 60, 324 349. Parre, E., Ghars, M.A., Leprince, A., Thiery, L., Lefebvre, D., 2007. Calcium signaling via phospholipase C is essential for proline accumulation upon ionic but not nonionic hyperosmotic stresses in Arabidopsis. Plant Physiol. 144, 503 512. Pastori, G.M., 2002. Common components, networks, and pathways of cross-tolerance to stress. The central role of “Redox” and abscisic acid-mediated controls. Plant Physiol. 129, 460 468. Patel, A., Khare, P., Patra, D.D., 2017. Biochar mitigates salinity stress in plants. Plant Adaptation Strategies in Changing Environment. pp. 153 182. Per, T.S., Khan, N.A., Sudhakar, P., Masood, A., Hasanuzzaman, M., Khan, M.I.R., et al., 2017. Plant Physiology and Biochemistry approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics. Plant Physiol. Biochem. 115, 126 140. Perera, L.K.R.R., Robinson, M.F., Mansfield, T.A., 1995. Responses of the stomata of Aster tripolium to calcium and sodium ions in relation to salinity tolerance. J. Exp. Bot. 46, 623 629. ˇ unek, ˚ Phogat, V., Pitt, T., Cox, J.W., Sim J., Skewes, M.A., 2018. Soil water and salinity dynamics under sprinkler irrigated almond exposed to a varied salinity stress at different growth stages. Agric. Water Manage. 201, 70 82. Pilon-Smits, E., 2005. Phytoremediation. Annu. Rev. Plant Biol. 56, 15 39. Porcel, R., Aroca, R., Ruiz-Lozano, J.M., 2011. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev. 32, 181 200. Qadir, M., Schubert, S., 2002. Degradation processes and nutrient constraints in sodic soils. L. Degrad. Dev. 13, 275 294. Qadir, M., Noble, A.D., Schubert, S., Thomas, R.J., Arslan, A., 2006. Sodicity-induced land degradation and its sustainable management: problems and prospects. L. Degrad. Dev. 17, 661 676.

Plant Life under Changing Environment

72

3. Salinity and its tolerance strategies in plants

Qadir, M., Oster, J.D., Schubert, S., Noble, A.D., Sahrawat, K.L., 2007. Phytoremediation of sodic and saline-sodic soils. Adv. Agron. 96, 197 247. Quirk, J.P., 2001. No title Aust. J. Soil Res. 39, 1185. Qureshi, A.S., McCornick, P.G., Qadir, M., Aslam, Z., 2008. Managing salinity and waterlogging in the Indus Basin of Pakistan. Agric. Water Manage. 95, 1 10. Rady, M.M., Taha, R.S., Mahdi, A.H.A., 2016. Proline enhances growth, productivity and anatomy of two varieties of Lupinus termis L. grown under salt stress. S. Afr. J. Bot. 102, 221 227. Rahnama, A., James, R.A., Poustini, K., Munns, R., 2010. Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Funct. Plant Biol. 37, 255 263. Rais, L., Masood, A., Inam, A., Khan, N., 2013. Sulfur and nitrogen coordinately improve photosynthetic efficiency, growth and proline accumulation in two cultivars of mustard under salt stress. J. Plant Biochem. Physiol. 1, 1 6. Rasool, S., Hameed, A., Azooz, M.M., Muneeb-u-Rehman, Siddiqi, T.O., Ahmad, P., 2012. Salt stress: causes, types and responses of plants. Ecophysiology and Responses of Plants under Salt Stress. Rasouli, F., Kiani Pouya, A., Karimian, N., 2013. Wheat yield and physico-chemical properties of a sodic soil from semi-arid area of Iran as affected by applied gypsum. Geoderma 193 194, 246 255. Raza, Z.I., Rafiq, M.S., Rauf, A., 2001. Gypsum application in slots for reclamation of saline-sodic soils. Int. J. Agric. Biol 3, 281 285. Rehman, M.Z., Murtaza, G., Qayyum, M., Saqib, M., Akhtar, J., 2017. Salt-affected soils: sources, genesis and management. Soil science concept and applications. University of Agriculture Faisalabad, pp. 191 216. Rengasamy, P., 2006. World salinization with emphasis on Australia. J. Exp. Bot. 57, 1017 1023. Rengasamy, P., 2010. Soil processes affecting crop production in salt-affected soils. Funct. Plant Biol. 37, 613. Rengasamy, P., 2016. Soil salinization. Oxford Res. Encycl. Environ. Sci. Oxford University Press, USA. Rodrigues, M.A., Bianchetti, R.E., Freschi, L., 2014. Shedding light on ethylene metabolism in higher plants. Front. Plant Sci. 5, 665. Roy, S.J., Negra˜o, S., Tester, M., 2014. Salt resistant crop plants. Curr. Opin. Biotechnol . Ryu, C.-M., Hu, C.-H., Locy, R.D., Kloepper, J.W., 2005. Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268, 285 292. Saifullah, D.S., Naeem, A., Rengel, Z., Naidu, R., 2018. Biochar application for the remediation of salt-affected soils: Challenges and opportunities. Sci. Total Environ. 625, 320 335. Saha, P., Banerjee, A., Sarkar, S., 2014. Phytoremediation potential of duckweed (Lemna minor L.) on steel wastewater. Int. J. Phytoremediation 17, 589 596. Sa´nchez-Blanco, M.J., Morales, M.A., Torrecillas, A., Alarco´n, J.J., 1998. Diurnal and seasonal osmotic potential changes in Lotus creticus creticus plants grown under saline stress. Plant Sci. 136, 1 10. Saqib, M., Zo¨rb, C., Rengel, Z., Schubert, S., 2005. The expression of the endogenous vacuolar Na1/H1 antiporters in roots and shoots correlates positively with the salt resistance of wheat (Triticum aestivum L.). Plant Sci 169, 959 965. Sarkar, A., Ghosh, P.K., Pramanik, K., Mitra, S., Soren, T., Pandey, S., et al., 2018. A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res. Microbiol. 169, 20 32. Sastre-Conde, I., Carmen Lobo, M., Icela Beltra´n-Herna´ndez, R., Poggi-Varaldo, H.M., 2015. Remediation of saline soils by a two-step process: washing and amendment with sludge. Geoderma 247 248, 140 150. Schroeder, J.I., Delhaize, E., Frommer, W.B., Guerinot, M.L., Harrison, M.J., Herrera-Estrella, L., et al., 2013. Using membrane transporters to improve crops for sustainable food production. Nature 497, 60 66. Scotti, R., Bonanomi, G., Scelza, R., Zoina, A., Rao, M.A., 2015. Organic amendments as sustainable tool to recovery fertility in intensive agricultural systems. J. Soil Sci. Plant Nutr. 15, 333 352. Sehrawat, N., Bhat, K.V., Sairam, R.K., Tomooka, N., Kaga, A., Shu, Y., et al., 2013. Diversity analysis and confirmation of intra-specific hybrids for salt tolerance in mungbean (Vigna radiata L. Wilczek). Int. J. Integr. Biol. 14, 1465 1473. Serrano, R., Rodriguez-Navarro, A., 2001. Ion homeostasis during salt stress in plants. Curr. Opin. Cell Biol. 13, 399 404. Seung, D., Risopatron, J.P.M., Jones, B.J., Marc, J., 2011. Circadian clock-dependent gating in ABA signalling networks. Protoplasma 249, 445 457.

Plant Life under Changing Environment

References

73

Shaaban, M., Abid, M., Rai, A.-S., 2013. Amelioration of salt affected soils in rice paddy system by application of organic and inorganic amendments. Plant Soil Environ. 59, 227 233. Shah, S.H., Houborg, R., McCabe, M., 2017. Response of chlorophyll, carotenoid and SPAD-502 measurement to salinity and nutrient stress in wheat (Triticum aestivum L.). Agronomy 7, 61. Shahbaz, M., Ashraf, M., 2013. Improving salinity tolerance in cereals. CRC. Crit. Rev. Plant Sci. 32, 237 249. Sharma, S., Kulkarni, J., Jha, B., 2016. Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front. Microbiol. 7, 1600. Sha Valli Khan, P.S., Nagamallaiah, G.V., Dhanunjay Rao, M., Sergeant, K., Hausman, J.F., 2014. Abiotic stress tolerance in plants. Emerg. Technol. Manag. Crop Stress Toler. Sheng, M., Tang, M., Zhang, F., Huang, Y., 2010. Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21, 423 430. Shrivastava, P., Kumar, R., 2015. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 22, 123 131. Shukla, P.S., Agarwal, P.K., Jha, B., 2011. Improved salinity tolerance of Arachis hypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J. Plant Growth Regul. 31, 195 206. Silva, P., Fac¸anha, A.R., Tavares, R.M., Gero´s, H., 2009. Role of tonoplast proton pumps and Na1/H1 antiport system in salt tolerance of Populus euphratica Oliv. J. Plant Growth Regul. 29, 23 34. Simonson, R.W., 1995. Factors of soil formation. A system of quantitative pedology. Geoderma 68, 334 335. Singh, K., 2015. Microbial and enzyme activities of saline and sodic soils. L. Degrad. Dev. 27, 706 718. Solmaz, I., Sari, N., Dasgan, Y., Aktas, H., Yetisir, H., Unlu, H., 2011. The effect of salinity on stomata and leaf characteristics of dihaploid melon lines and their hybrids. J. Food Agri. Environ 9, 172 176. Stepien, P., Johnson, G.N., 2008. Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol. 149, 1154 1165. ´ P., Kłbus, G., 2006. Water relations and photosynthesis in Cucumis sativus L. leaves under salt stress. Biol. Ste˛pien, Plant. 50, 610 616. Stewart, C.R., 1980. The mechanism of abscisic acid-induced proline accumulation in barley leaves. Plant Physiol. 66, 230 233. Strizhov, N., Abraha´m, E., Okre´sz, L., Blickling, S., Zilberstein, A., Schell, J., et al., 1997. Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J. 12, 557 569. Sua´rez, N., Medina, E., 2008. Salinity effects on leaf ion composition and salt secretion rate in Avicennia germinans (L.) L. Braz. J. Plant Physiol. 20, 131 140. Sudhir, P., Murthy, S.D.S., 2004. Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42, 481 486. Sunkar, R., Zhu, J.-K., 2007. Micro RNAs and short-interfering RNAs in plants. J. Integr. Plant Biol. 49, 817 826. Suzuki, K., Yamaji, N., Costa, A., Okuma, E., Kobayashi, N.I., Kashiwagi, T., et al., 2016. OsHKT1;4-mediated Na1 transport in stems contributes to Na1 exclusion from leaf blades of rice at the reproductive growth stage upon salt stress. BMC Plant Biol 16, 22. Tabot, P.T., Adams, J.B., 2014. Salt secretion, proline accumulation and increased branching confer tolerance to drought and salinity in the endemic halophyte Limonium linifolium. S. Afr. J. Bot. 94, 64 73. Taffouo, V.D., Wamba, O.F., Youmbi, E., Nono, G.V., Akoa, A., 2010. Growth, yield, water status and ionic distribution response of three bambara groundnut (Vigna subterranea (L.) Verdc.) landraces grown under saline conditions. Int. J. Bot. 6, 53 58. Tarte, V.N., Seok, H.Y., Woo, D.H., Le, D.H., Tran, H.T., Baik, J.W., et al., 2015. Arabidopsis Qc-SNARE gene AtSFT12 is involved in salt and osmotic stress responses and Na1 accumulation in vacuoles. Plant Cell Rep. 34, 1127 1138. Tavarini, S., Cardelli, R., Saviozzi, A., Degl’Innocenti, E., Guidi, L., 2011. Effects of green compost on soil biochemical characteristics and nutritive quality of leafy vegetables. Compost Sci. Util. 19, 114 122. Tejada, M., Garcia, C., Gonzalez, J.L., Hernandez, M.T., 2006. Use of organic amendment as a strategy for saline soil remediation: influence on the physical, chemical and biological properties of soil. Soil Biol. Biochem. 38, 1413 1421.

Plant Life under Changing Environment

74

3. Salinity and its tolerance strategies in plants

Tejada, M., Hernandez, M.T., Garcia, C., 2009. Soil restoration using composted plant residues: effects on soil properties. Soil Tillage Res. 102, 109 117. Tofighi, C., Khavari-Nejad, R.A., Najafi, F., Razavi, K., Rejali, F., 2017. Brassinosteroid (BR) and arbuscular mycorrhizal (AM) fungi alleviate salinity in wheat. J. Plant Nutr. 40, 1091 1098. Tracy, F.E., Gilliham, M., Dodd, A.N., Webb, A.A.R., Tester, M., 2008. NaCl-induced changes in cytosolic free Ca2 in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant Cell Environ. 31, 1063 1073. Trnka, M., Kersebaum, K.C., Eitzinger, J., Hayes, M., Hlavinka, P., Svoboda, M., et al., 2013. Consequences of climate change for the soil climate in Central Europe and the central plains of the United States. Clim. Change 120, 405 418. Turan, S., 2018. Single-gene versus multigene transfer approaches for crop salt tolerance, Salinity Responses and Tolerance in Plants, vol.1. Turkan, I., 2018. ROS and RNS: key signalling molecules in plants. J. Exp. Bot 69, 3313. Tuteja, N., 2007. Mechanisms of high salinity tolerance in plants. Methods Enzymol. 428, 419 438. Valzano, F.P., Greene, R.S.B., Murphy, B.W., 1997. Direct effects of stubble burning on soil hydraulic and physical properties in a direct drill tillage system. Soil Tillage Res. 42, 209 219. Van Beek, C.L., To´th, T., Hagyo´, A., To´th, G., Recatala´ Boix, L., An˜o´ Vidal, C., et al., 2010. The need for harmonizing methodologies for assessing soil threats in Europe. Soil Use Manage. 26, 299 309. Verslues, P.E., Bray, E.A., 2005. Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J. Exp. Bot. 57, 201 212. Vishwakarma, K., Upadhyay, N., Kumar, N., Yadav, G., Singh, J., Mishra, R.K., et al., 2017. Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant Sci. 08, 1 12. Vurukonda, S.S.K.P., Vardharajula, S., Shrivastava, M., SkZ, A., 2016. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol. Res 184, 13 24. Walker, D.J., Bernal, M.P., 2008. The effects of olive mill waste compost and poultry manure on the availability and plant uptake of nutrients in a highly saline soil. Bioresour. Technol 99, 396 403. Wang, B., Lu¨ttge, U., Ratajczak, R., 2001. Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J. Exp. Bot 52, 2355 2365. Wang, W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1 14. Wang, S.J., Chen, Q., Li, Y., Zhuo, Y.Q., Xu, L.Z., 2017. Research on saline-alkali soil amelioration with FGD gypsum. Resour. Conserv. Recycl. 121, 82 92. Wang, Y., Deng, C., Liu, Y., Niu, Z., Li, Y., 2018. Identifying change in spatial accumulation of soil salinity in an inland river watershed, China. Sci. Total Environ. 621, 177 185. Warren, S.D., 2001. Synopsis: influence of biological soil crusts on arid land hydrology and soil stability. Biological soil crusts: Structure, function, and management. Springer, Berlin, Heidelberg, pp. 349 360. Weigel D. and Glazebrook J., EMS mutagenesis of Arabidopsis seed. Cold Spring Harbor Protocols, 2006 (5), pp.pdbprot4621. White, P.J., Brown, P.H., 2010. Plant nutrition for sustainable development and global health. Ann. Bot. 105, 1073 1080. Wicke, B., Smeets, E., Dornburg, V., Vashev, B., Gaiser, T., Turkenburg, W., et al., 2011. The global technical and economic potential of bioenergy from salt-affected soils. Energy Environ. Sci. 4, 2669 2681. Wong, V.N.L., Greene, R.S.B., Dalal, R.C., Murphy, B.W., 2009. Soil carbon dynamics in saline and sodic soils: a review. Soil Use Manage. 26, 2 11. Woodward, A.J., Bennett, I.J., 2005. The effect of salt stress and abscisic acid on proline production, chlorophyll content and growth of in vitro propagated shoots of Eucalyptus camaldulensis. Plant Cell, Tissue and Organ Culture 82, 189 200. Wu, C.-A., Yang, G.-D., Meng, Q.-W., Zheng, C.-C., 2004. The cotton GhNHX1 gene encoding a novel putative tonoplast Na1/H1 antiporter plays an important role in salt stress. Plant Cell Physiol. 45, 600 607. Wungrampha, S., Joshi, R., Singla-Pareek, S.L., Pareek, A., 2018. Photosynthesis and salinity: are these mutually exclusive? Photosynthetica 56, 366 381. Yadav, H., Fatima, R., Sharma, A., Mathur, S., 2017. Enhancement of applicability of rock phosphate in alkaline soils by organic compost. Appl. Soil Ecol. 113, 80 85.

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Further reading

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Yamaguchi, T., Blumwald, E., 2005. Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci. 10, 615 620. Yamaguchi-Shinozaki, K., Shinozaki, K., 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781 803. Yin, Y.G., Tominaga, T., Iijima, Y., Aoki, K., Shibata, D., Ashihara, H., et al., 2010. Metabolic alterations in organic acids and γ-aminobutyric acid in developing tomato (Solanum lycopersicum L.) fruits. Plant Cell Physiol 51, 1300 1314. Zapata, P.J., Serrano, M., Garcı´a-Legaz, M.F., Pretel, M.T., Botella, M.A., 2017. Short term effect of salt shock on ethylene and polyamines depends on plant salt sensitivity. Front. Plant Sci. 8, 855. Zhang, H.X., Blumwald, E., 2001. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat. Biotechnol. 19, 765 768. Zhang, J.L., Shi, H., 2013. Physiological and molecular mechanisms of plant salt tolerance. Photosynth. Res. 115, 1 22. Zhang, J.L., Flowers, T.J., Wang, S.M., 2010. Mechanisms of sodium uptake by roots of higher plants. Plant Soil 326, 45. Zhou, C., Zhu, L., Xie, Y., Li, F., Xiao, X., Ma, Z., et al., 2017. Bacillus licheniformis SA03 Confers Increased Saline Alkaline Tolerance in Chrysanthemum Plants by Induction of Abscisic Acid Accumulation. Front. Plant Sci 8, 1143. Zhu, T., Deng, X., Zhou, X., Zhu, L., Zou, L., Li, P., et al., 2016. Ethylene and hydrogen peroxide are involved in brassinosteroid-induced salt tolerance in tomato. Sci. Rep 6, 35392. Zhu, J.K., 2001. Plant salt tolerance. Trends Plant Sci. 6, 66 71. Zhu, J.K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247 273. Zhu, J.K., 2003. Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 6, 441 445.

Further reading Blumwald, E., 2000. Sodium transport and salt tolerance in plants. Curr. Opin. Cell Biol. 12, 431 434. Brown, A.D., 1983. Halophilic prokaryotes. Physiological Plant Ecology III. Springer, Berlin, Heidelberg. Carvalho, D.R.A., Fanourakis, D., Correia, M.J., Monteiro, J.A., Arau´jo-Alves, J.P.L., Vasconcelos, M.W., et al., 2016. Root-to-shoot ABA signaling does not contribute to genotypic variation in stomatal functioning induced by high relative air humidity. Environ. Exp. Bot. 123, 13 21. Carvalho, D.R.A., Vasconcelos, M.W., Lee, S., Vreugdenhil, D., Heuvelink, E., Carvalho, S.M.P., 2017. Moderate salinity improves stomatal functioning in rose plants grown at high relative air humidity. Environ. Exp. Bot. 143, 1 9. de la Paix, M.J., Lanhai, L., Xi, C., Varenyam, A., Nyongesah, M.J., Habiyaremye, G., 2011. Physicochemical properties of Saline soils and aeolian dust. L. Degrad. Dev. 24, 539 547. Farouk, S., Amany, A.R., 2012. Improving growth and yield of cowpea by foliar application of chitosan under water stress. Egypt. J. Biol. 14, 14 26. Freitas, V.S., de Souza Miranda, R., Costa, J.H., de Oliveira, D.F., de Oliveira Paula, S., de Castro Miguel, E., et al., 2018. Ethylene triggers salt tolerance in maize genotypes by modulating polyamine catabolism enzymes associated with H2O2 production. Environ. Exp. Bot. 145, 75 86. Fuller, R., 2015. Resilience in Pakistan: Evaluation of Enhancing Food Security and Resilience of Small-Scale Farmers. Oxfam GB. Indira, E., Annadurai, B., 2016. Impact of farm yard manure and goat manure as organic amendment on physicochemical and physical properties of theri soil. Int. J. Plant Soil Sci. 9, 1 6. Kibria, M.G., Hossain, M., Murata, Y., Hoque, M.A., 2017. Antioxidant defense mechanisms of salinity tolerance in rice genotypes. Rice Sci. 24, 155 162. Lim, T.J., Spokas, K.A., Feyereisen, G., Novak, J.M., 2016. Predicting the impact of biochar additions on soil hydraulic properties. Chemosphere 142, 136 144. Mandal, S., Dutta, P., Umdar, S.M.A.J., 2017. Plant growth promoting and antagonistic activity of Bacillus strains isolated from rice rhizosphere. Int. J. pharma Bio Sci. 8, 408 415. Mitnala, J., 2018. Performance of sugarcane varieties with respect of growth parameters and their management in sodic soil. Res. J. Agric. Biol. Sci 6, 322 325.

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Munns, R., 2002. Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239 250. Nirmala, S., Mukesh, Y., Venkataraman, B.K., Kumar, S.R., Kumar, J.P., 2016. Hybridization between salt resistant and salt susceptible genotypes of mungbean (Vigna radiata L. Wilczek) and purity testing of the hybrids using SSRs markers. J. Integr. Agric. 15, 521 527. Pardo, J.M., Quintero, F.J., 2002. No title. Genome Biol. 3, reviews1017.1. Patel, A.D., Pandey, A.N., 2008. Growth, water status and nutrient accumulation of seedlings of Holoptelea integrifolia (Roxb.) planch in response to soil salinity. Plant Soil Environ. 54, 367 373. Poulain, D., 1984. Influence of density on the growth and development of winter field bean (Vicia faba). Vicia faba: Agronomy, Physiology and Breeding. Springer, Dordrecht. Walsh, G.E., Barrett, R., Cook, G.H., Hollister, T.A., 1973. Effects of herbicides on seedlings of the red mangrove, Rhizophora mangle L. Bioscience 23, 361 364. Richards, L., 1954. Diagnosis and Improvement of Saline and Alkali Soils: Soil Science (WWW Document). LWW. Sari, N., Solmaz, I., Yetisir, H., Unlu, H., 2007. Watermelon genetic resources in Turkey and their characteristics. Acta Hortic. 371, 433 438. Shah, S.M., Rasmus, H., McCabe, M.F., 2017. Response of chlorophyll, carotenoid and SPAD-502 measurement to salinity and nutrient stress in wheat (Triticum aestivum L.). Agronomy 7, 61. Teuscher, G., 1968. Thema: Deutschland; Edited by Edward C. Breitenkamp. Prentice-Hall German Series, 1967. Prentice-Hall, Inc., Englewood Cliffs, New Jersey. Can. Mod. Lang. Rev. 24, 100b 101. Wada, K.C., Takeno, K., 2013. Salicylic acid-mediated stress-induced flowering. Salicylic Acid. Springer, Dordrecht, 163 182. Yu, Z.-D., Wang, L.-N., Cao, C.-X., Hu, X.Y., 2010. The effects of exogenous nitric oxide on growth, active oxygen metabolism and photosynthetic characteristics in cucumber (Cucumis sativus) seedlings under cadmium stress. Acta Bot. Yunnanica 31, 486 492.

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C H A P T E R

4 Regulation of drought stress in plants Zia Ur Rahman Farooqi, Muhammad Ashar Ayub, Muhammad Zia ur Rehman, Muhammad Irfan Sohail, Muhammad Usman, Hinnan Khalid and Komal Naz Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan

4.1 Introduction Drought is one of the major factors affecting crop production worldwide as crop growth is significantly affected by this stress so does the yield. Drought stress mainly occurs due to the less rainfall, salt accumulation in soil, extreme temperature fluctuations, and high intensity of light. Climate simulation models that take in to account previous year data and simulate future have predicted that this stress will be more severe in near future due to climate change. Drought stress primarily impairs the normal plant growth, disturbs its water retention, and reduces water-use efficiency (Fathi and Tari, 2016) and can cause changes in the physiological, biochemical, morphological, and molecular traits in plants. Drought-tolerant/resistant plants have evolved an improved drought resilience mechanism to tolerate drought stress, though very efficient but these mechanisms are not well organized and well-studied. Generally, plants show mechanism of maintaining cell homeostasis, which is done by increasing water movement into plant cell. “Drought resistance” is another mechanism of cellular defense against drought to escape drought prevailing long periods (Salehi-Lisar and Bakhshayeshan-Agdam, 2016; Basu et al., 2016). Besides drought tolerance, plants tend to adopt many metabolic changes to cope with drought stress such as decrease in ribulose bisphosphate (RuBP) and adenosine triphosphate (ATP) contents and decrease in Rubisco activity. During drought, plants tend to avoid water loss up to its maximum capacity by decreasing substomatal CO2 conductance and closing stomata (Flexas and Medrano, 2002). Water stress also affect plant by decreasing its light saturation rate, decarboxylation velocity, ribulose 1,5-bisphosphate regeneration capability, photosystem II (PS-II) efficiency, and stomatal conductance (Flexas et al., 2004). Amino acids, such as asparagine and glutamic acid, in plants are also severely affected by drought, but plant can respond to this change by immediately increasing amino acids and

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00004-7

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soluble contents to mitigate stress momentarily and manage osmotic potential (Aranjuelo et al., 2010; Pinheiro and Chaves, 2010). Other major mechanisms for combating with drought stress include increase in diffusive resistance, enhancing water uptake, and extending roots growth to reach maximum depth and absorb water effectively, and succulent leaf development over time. Nutritional management of drought stress involves osmotic adjustment using potassium ion and cell wall stiffening by the silicification by silicon, which helps improve cellular water balance. During water deficit conditions, low molecular-weight osmolytes, such as glycine betaine, proline, organic acids, polyols, and other amino acids, play a crucial role in cellular functioning under drought stress. Plants under stress tend to produce polyamines, citrulline, and several other enzymes, which act as antioxidants to reduce reactive oxygen species (ROS) production initiated by water deficit. At cellular level, plants switch on several drought-responsive genes and/or transcription factors as dehydration-responsive-elementbinding gene, embryogenesis-abundant proteins and dehydrins. For a sustainable and long-lasting drought combating, plant breeding, genetic engineering, marker-assisted selection, and exogenous application of osmo-protectants and hormones application are suitable options (Farooq et al., 2012; Lin et al., 2013; Xu et al., 2010; de Souza et al., 2015). This chapter is an effort to summarize causes and impacts of drought, how it influences plant growth, and how plants tend to adopt, or we make them adopt drought to assure sustainable crop production in changing climatic conditions.

4.2 Causes of drought Climate is one of the most important factors in the environment, which can affect all the activities of the environment (IEA, 2015). Severe droughts are the result of climate change. Cropping pattern and plant growth are also affected by the climate and weather (Iizumi and Ramankutty, 2015). Climate change affects the water availability for crop production and drinking purposes (Elliott et al., 2014). Warm temperature for a longer period increases the duration of drought in the West America (Andreadis and Lettenmaier, 2006). The increase in temperature leads to more precipitation instead of snow falling because snow melts earlier and increases the evapotranspiration (Stigter et al., 2017). With the rise in temperature, the risk for agricultural drought also increases. Climate change has been affecting the snowpack of the West Mountain since the mid-century (Mote, 2006). This has resulted to reduction in snow falling and change the snow melting time (Salzmann et al., 2014). In Europe in 2003, drought was mainly caused by the rise in temperature that led to approximately 30% decrease in net productivity in Western and Eastern Europe (Ciais et al., 2005). The rise in temperature for a longer period of time causes the loss of moisture from the soil (Berg et al., 2014). The frequency can be double because of greenhouse gases and excessive global warming. The emission of greenhouse gases is increasing day by day, which leads to rise in temperature (Zickfeld et al., 2017). This leads to change in climate, disturbance in the weather pattern, and alteration in precipitation patterns due to ocean circulations such as “La Nin˜a and El-Nino,” which regulate the global temperatures (Cook et al., 2007). In addition to the above-mentioned reasons, human activities—such as deforestation, decreasing depth of groundwater and depletion in surface water supply,

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overgrazing and overexploitation of natural resources, such as, water—have resulted in the enhancement of drought (Gurmu and Mace, 2008). Based upon the statistical data of last 60 years, Duran-Encalada et al. (2017) stated that scarcity of water was due to the climate change causing high temperatures and depletion of water resources gradually. Prevailing El Nin˜o conditions is also responsible for drought conditions, which causes reduction in rainfall up to 1.5 1.7 times, soil moisture, and hence creates groundwater depletion (van Dijk et al., 2013; Fang and Pomeroy, 2008). Deficiency of rainfall for a long period of time also causes drought, low rainfall leads to the lack of precipitation (Thomas and Prasannakumar, 2016). Prolonged duration of low rainfall, usually for more than one season, can cause dry condition and less availability of water, which finally lead to drought. In some cases, there is no rain in a month in many areas, but this condition is normal for those regions (Yang et al., 2017b). While in other areas, agricultural land faces drought due to lack of proper irrigation infrastructure (Chai et al., 2016). The water cycle managed by human activities is relatively significant (Lu et al., 2016). Deforestation, building construction, and agricultural practices negatively affect the water cycle (Spera et al., 2016). Green vegetation provides a cover, which is necessary for water cycle, and also limits the evaporation of stored water; trees in forest also attract rain (Berland et al., 2017). In this perception, forest cutting and clearing the vegetation cover ¨ zkan increase the water evaporation and also reduce the ability of soil to hold water (O and Go¨kbulak, 2017). This leads to the occurrence of dry situation and reduces the watershed potential of forests (Sunderland et al., 2015). Human activities also directly cause drought due to overcropping and unnecessary use of water for irrigation purposes (Ren et al., 2016). Streams, rivers, and lakes are primary sources of surface waters in many regions of the world. The available supply of water is less than the demand of water, in the high temperature, and some human activities make the surface water dry and hence lead to drought conditions (Wan et al., 2017). Construction of dams and irrigation system are significantly reducing the surface water.

4.3 Impacts of drought A complex chain of impacts is produced by drought, which spans many sectors of economy (Hao and Singh, 2015). The complexity is due to the less availability of water. The impacts are mentioned as direct and indirect, which include reduction in crop production (Lesk et al., 2016), reduction in rangeland (Breshears et al., 2016), less productive forests (Helman et al., 2017), increase in fire hazard (Littell et al., 2016), decrease in water level (Fang and Xiong, 2015), increase in the death rate of wildlife (Seabrook et al., 2011), livestock, and also damage to fishes (FAO, 2014). The indirect impacts depend on direct ones, such as the reduction in the productivity of agricultural commodities and forests and reduction in the rangeland may result in the reduction of income of farmers and agricultural businessmen (FAO, 2014), increase in the prices of agricultural products (Liu et al., 2016), increase in unemployment rate (Levine, 2013), and reduction in the tax revenues (Ramı´rez et al., 2017).

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Drought affects the environment and all the communities present in the environment. Water is a basic component of the environment; hence, loss of water affects the all living and nonliving things of the environment. Like human, animals and plants totally depend on water. The supply of food shrinks, and the habitats of animals and plans are also damaged by drought. Due to deterioration in wildlife and fish habitat (FAO, 2014), less availability of food (Calow et al., 2010) and water, diseases increase in animals, wild animals migrate (Mosley, 2015), and wetlands reduce because of poor quality of soil and the erosion of soil. All these factors form an environment, and if the water content is low, it affects the environment ultimately (Fang and Xiong, 2015). Shortage of food and damage to their habitat are a temporary effect, they return to normalcy when the duration of drought is completed. But in some cases, the environment is affected by drought for longer period of time or may be forever. Drought causes damage to the plant and animal species, habitat of wildlife, quality of air, forests and rangeland and the quality of landscape. All these temporary effects of drought may return to normalcy after a period of time. But some of the areas are permanently affected by drought causing loss of soil fertility due to wind erosion of soil which may lead to permanent loss of biodiversity (Mosley, 2015). Drought indirectly affects the economy of people by damaging the plants and animals in the environment. It leads to less supply of water to produce crops, and the farmers spend a lot of money for the irrigation of agricultural field and the establishment of new tube wells. Animal farm managers also spend money to pay for feed and water for their livestock (Kay, 1997). Due to the effect of drought on crops and animals, businesses that depend on agricultural commodities and companies engaged in the manufacturing of tractors and food face losses in their respective businesses. Similarly if the forests are damaged by drought, people working with timber and in the timber industries are majorly affected. There are many difficulties in import and export through oceans and sea due to the low level of water. Electricity generated by water, that is, hydroelectric power, is also disturbed by the low availability of water, and people have to spend more money for electricity. All these scenarios lead to the increase in unemployment, credit risk for financial institutes, and shortfalls of capital, which eventually leads to revenue loss of the government. In certain cases, because of less production of food due to drought, food products are imported from the other states to fulfill the demand, and a huge amount of money is also spent, which can also significantly affect the economy of the country (Salami et al., 2009). By nature, human is a social animal so it relates with other human and its environment. These relations go well until they have no health issues or other problems. But due to drought, human suffers from scarcity of food, health safety and has conflict over water use (Carolina et al., 2002), which leads to social imbalance and affects the quality of life. Social impacts are related with the environmental and economic impacts. Migration of population is a significant problem of many countries that face drought. Migration occurs often to urban areas from stressed areas or the regions outside the stress area. This may lead to increase in poverty and pressure on the urban social infrastructure (Wanders and Wada, 2015). Drought causes depression, anxiety, health problems, and loss of human health due to loss of economy, poor quality of water and dust.

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4.3.1 Impact on global agriculture In Mexico, drought conditions have resulted in the loss of agricultural productivity, thus affecting economy. These losses are higher at large private farms (Liverman, 1990). Drought changes the cloud cover and rainfall pattern and promotes fire (Asner and Alencar, 2010). It can lead to potentially large and highly differentiated impacts on global level depending upon the structure and economy of affected states or countries. A country’s economy adversely gets affected based on the extent and severity of drought, and policy makers keeping that in mind, provide relief and mitigate drought stress (Benson and Clay, 1994). Drought is also involved in the reduction of area under cultivation and hence one of the major causes that reduces the crop productivity, raising the problem of food security (Kang et al., 2009). 4.3.1.1 Impacts on individual plant Water is a necessary commodity for life as it forms a major portion of plant and animal cell bodies. In the absence of water, all the life-sustaining processes, such as photosynthesis, plant growth, including root and plant growth, result in progressive cell deaths. Drought has drastic effects on environment and plants life, as it affects the seed germination, plant growth, phenology, nutrient availability, photosynthesis, and respiration. All these processes are much important in plant life cycle that if a single process is missed, whole plant will get affected and show the symptoms of this effect. In addition to the major threats, drought stress can reduce leaf size and stem extension, root proliferation as well as adversely disturb plant water relations/water-use efficiency due to which plants show a variety of biochemical and physiological responses (Farooq et al., 2009). Drought stress causes burning of forests, which ultimately reduces the carbon sinks, and releases carbon by forest-biomass decomposition (Kolb et al., 2013). Plant growth is affected by many environmental factors such as biotic and abiotic (Pandey et al., 2017). Among abiotic factors, drought affects the plant growth worldwide. In the environment, water is lost by the light intensity (da Silva Branco et al., 2017), increase in temperature (Yamaguchi et al., 2011), less relative humidity (Masaki et al., 2015), and high speed of wind (Schymanski and Or, 2015). Shortage of water decreases the stomatal conductance (Maes et al., 2011), loss of turgor in leaves (Boyer, 2015), structure of organ (Wu and Tan, 2012), photosynthetic rate, and transpiration rate (Li et al., 2017), and also generates the ROS (Miller et al., 2010) and causes enzymatic stress in the cells of leaves such as increase the production of superoxidase (Aslam et al., 2013). Photosynthesis is the most important process for plants. The yield of plant also deteriorates by the reduction in the process of photosynthesis (Zargar et al., 2017). Shortage of water turns the leaves of some species in blue-green (Saleska et al., 2007). If water is unavailable to plants for a longer period, foliage plants wilt and lose its leaves considerably, and as a result plants die. Initially recognized symptom of water stress is wilting, because the water pressure inside leaves decreases and plants undergo wilt condition (Zeppel et al., 2015). Water is essential to control the temperature of a plant body. Most of the water is lost through stomatal transpiration which is greater than the stored amount in the plant cells. This loss of water cools the leaves; it causes the inactivation of enzyme activity, related to

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photosynthesis and respiration in the leaves because it will become too warm. Plants cannot maintain their body temperature while they face water shortage (Adams et al., 2009). Due to drought conditions, the plant canopy gets damaged, which leads to less absorption of radiation energy, which increases the plant yield. As a result the grain yield is reduced as well as the number of grains per plant (Shahattary and Mansourifar, 2017). Under water stress conditions, a relative growth rate of plant reduces, and the plant height also decreases (Lipiec et al., 2013). In addition, plant biomass is affected due to the scarcity of water; as a result, fresh and dry weight of plants is reduced (Lipiec et al., 2013). Many researchers reported that the production of oil increases by reducing irrigation water. The percentage of grain oil yield is increased by drought stress but decreased by severe drought stress (Mozaffari and Asadi, 2006). Due to water scarcity, the number of grains per follicles is reduced in the oil seed crops; also grain biomass, the number of grains per capsules, and the capsule number per plant decrease due to water shortage (Lipiec et al., 2013). Grain weight is also reduced by drought stress significantly. All these are related to photosynthetic activities, which also reduce the number of fertilized flower, the abortion of leaves during flowering stage, subsequent grain reduction, and considerably the yield (Rezaei et al., 2012). Deficiency of water reduces the growth of plants, surface area of leaves, dry matter; it also leads to a deterioration of cell membrane, damage of pigments, reduction in chlorophyll contents, and a damage of root growth. For drought stress, herbal tissues of the plants are also damaged (Farooq et al., 2009). 4.3.1.1.1 Metabolic changes

Drought stress affects the metabolic process of plants and increases the secondary metabolites that are protective against drought stress (Walter et al., 2012). The amount of soluble protein increases with increasing drought stress in tolerant species of plants. But in sensitive genotypic plants, the soluble protein decreases with the increase in the drought stress. Soluble protein is responsible for maintaining the plant structure, so the decrease in the soluble protein production changes the plant structure (Wehner et al., 2015). Carbohydrate, water, fats proline, and vitamins are the components that are responsible for better plant growth. They are interconnected to each other, so deficiencies in any one of them affect the plant mechanism (Fang and Xiong, 2015). Balance in water and proline synthesis is very important for balanced functioning of plants. But in drought conditions, less water is available for the plant growth and increases the proline synthesis. Drought stress also increases the ornithine aminotransferase activity in plants, which is responsible for proline production (You et al., 2012). Due to the shortage of water, so for decrease in water solubility, the concentration of proline increases. The accumulation of proline in the cytoplasm indicates that plants face drought stress. Protein is important for cell as well as plant structures, and protein is also produced by proline in the plants. In tolerant plants, the proline synthesis increases with the increase in drought stress (Xoconostle-Ca´zares et al., 2010). Proline provides resistance against structure denaturation caused by drought stress. Plant cell structures are maintained by proline that is responsible for protein synthesis. It is regarded as the defense system of the plant under drought conditions. It is also helpful against the oxidative reduction in the plant cell. During drought stress, soluble sugar synthesis also increases in plant cells. Soluble sugars are the constituents of osmolytes which act as osmotic protection. As the soil

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moisture decreases, soluble sugar increases inside the plant cell (Vardharajula et al., 2011). Drought limits the crop growth, development, and yield processes (Prasad et al., 2008). Plants use mycorrhizal fungi to support itself for its growth. Mycorrhizal fungi play an important role in plant growth, and the production of flowers and fruits (Subramanian et al., 2006). Metabolic responses in drought stress include defense responses such as activation of multigene defense pathway and 454 transcripts, accumulation of sugars such as sucrose glucose and maltose in them (Rizhsky, 2004). Carbon dioxide equilibrium is also disturbed under drought condition, which is compensated by the increase of cuticular conductance and decreased mesophyll conductance (Flexas et al., 2004). RuBP and ATP contents decrease, and a decrease in photochemistry and Rubisco activity is also observed. Substomatal CO2 concentration lowers and stomata are closed (Flexas and Medrano, 2002). Drought stress also causes the decrease in light saturation rate, carboxylation extent, ribulose 1,5-bisphosphate regeneration capability, PS-II efficiency, and stomatal conductance (Nogue´s and Baker, 2000). Glutathione content decreases lipid peroxidation and causes reduction in PS-II photochemical efficiency and a higher increase in nonradiative energy dissipation (Loggini et al., 1999). Stress-responsive genes are expressed in response to the stress, which are about 15 in number in Arabidopsis thaliana and rice (Chaves et al., 2009). 4.3.1.1.2 Physiological changes

Photosynthesis, materials transfer, ion exchange, ion transfer, metabolism, and respiration are the series of biochemical and physiological processes involved in the plant growth (Zhu et al., 2013). These also influence plants’ dry weight (Seghatoleslami et al., 2008). The availability and continuity of water has direct relationship with all these processes (Zlotorowicz et al., 2017). As the amount of water is reduced, these processes are disturbed and plants unable to produce dry matter (Zlotorowicz et al., 2017). In drought conditions, water and nutrients uptake (Barbeta et al., 2015), also growth rate (Todaka et al., 2015) as well as plant growth time (Vicente-Serrano et al., 2013), height of plant (Todaka et al., 2015), physiological activities such as photosynthesis (Ashraf and Harris, 2013), and dry matter in plants are reduced (Todaka et al., 2015). The increase in the deficiency of water causes a reduction in plant biomass (Aranjuelo et al., 2010). Deficiency of water also disturbs the photosynthetic activity, which leads to reduction in the plant height (Todaka et al., 2015), leaf surface area (Greenwood et al., 2017), and photo assimilates accumulate in roots rather than aerial part of the plant (Hasibeder et al., 2015). Under drought conditions, leaf areas (Scoffoni et al., 2014), chlorophyll contents (Xiang et al., 2013), photosynthetic activity (Sperlich et al., 2015), grain filling duration are also lessened, and the prematurity of grain reduces the yield of plants. Photosynthesis is an important process in which water and carbon dioxide, in the presence of light, produce carbohydrates as energy sources. In the shortage of water, photosynthetic activity is reduced, which leads to a decrease in the growth and development. Water is a main component for the photosynthetic activity, but low availability of water brings some limitations, such as physical (Reddy et al., 2004). Stomata play an important role in photosynthesis in controlling the movement of water, carbon dioxide, and oxygen in and out of plant. Under drought conditions, stomata close for the conservation of water in the leaves. When stomata close, gaseous exchange pathways and transpiration reduce the photosynthesis rate (Berry et al., 2010). Shoot growth is more

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affected by drought stress than root growth because roots get relief under moisture stress (Pace et al., 1999). For less availability of water, photosynthesis negatively affects the energy synthesis, other cellular activities; plant growth rates are also reduced. Drought stress shows different effects in different plant species (Reddy et al., 2004). Some plants show a preservation of chlorophyll contents and photosynthetic duration under drought stress, which relates to the resistance of plants (Iovieno et al., 2016). Drought stress affects the electron transport chain, which initiates the production of ROS that are harmful for plant cells and organelles such as mitochondria, chloroplast, and peroxisomes. ROS also reduce and decompose the amount of chlorophylls in leaves (Zulini et al., 2007). In this process, chlorophylls decompose in chloroplast and damage the thylakoid structure. Chlorophyll-a, chlorophyll-b, and total chlorophyll contents get reduced by the deficiency of water, and it is observed considerably in the plants that do not face drought stress earlier. Reduction in chlorophyll contents destructs the chloroplast membrane and ultimately reduces the photosynthesis pigment’s concentration (Faraloni et al., 2011). Drought also affects plants by reducing carboxylation capacity, Rubisco content and activation state, and RuBP regeneration. It also decreases amino acid content such as asparagine and glutamic acid, and Rubisco protein content. But plants respond immediately and increase amino acid and intracellular soluble sugar contents to mitigate decreased osmotic potentials. In nodule forming plants, proline accumulation can also contribute toward osmoregulation response to drought and serve as a protector against ROS. Under drought, the decrease in N2 fixation is associated with increased oxygen resistance caused by ROS under drought stress (Aranjuelo et al., 2010).

4.4 Combating with drought Drought, as explained earlier, is a severe threat to environmental sustainability and vegetation. We need to adopt innovative strategies to cope with drought if we want a sustainable agriculture production for our planet. It is the need of hours worldwide to develop corporation to tackle drought more properly (Wilhite, 2002). Factors that are in control to maintain or cope with drought are described in the following sections.

4.4.1 Soil features 4.4.1.1 Soil biota activity Soil biota refers to living creatures of soil, which include microorganisms (bacteria, fungi), and soil fauna, which have diverse interaction with plants growing in that soil (Balestrini et al., 2015). Soil microbial mediated drought stress tolerance is well known and a widely studied phenomenon. Arbuscular mycorrhizae (AM) and soil bacteria help plants withstand water stress. Under drought stress, plants without symbiotic association with AM have higher stomatal conductance, superoxide dismutase (SOD) activities, but less tissue water contents compared to fungi-inoculated plants, which have better tolerance to drought stress (Ortiz et al., 2015). Similar to AM, autochthonous bacteria

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such as Bacillus thuringiensis have also reported to have drought amelioration impact on plants. This is a type of growth-promoting rhizobacteria, and it suppresses glutathione reductase and ascorbate peroxidase (POD) (APX) in inoculated Lavandula plants. Plant growth promoting rhizobacteria (PGPR) improve plant nutrition, biochemical activity, and physiological parameters (Armada et al., 2014). Drought ameliorating activities of PGPR, due to its nature of producing auxin and 1-aminocyclopropane-1-carboxylate (ACC) deaminase, help plants grow properly and bear/withstand abiotic stress by suppressing ethylene inside plants, and they can eliminate the usage of agrochemicals for combating water shortage (Lim and Kim, 2013). These compounds along with exopolysaccharides help plants in the accumulation of osmolytes, antioxidants and downregulate or upregulate stress-responsive gene for a better acquisition of drought tolerance (Vurukonda et al., 2016). 4.4.1.2 Soil physicochemical activities Soil physical properties have great influence on soil moisture content managements under scarce conditions. The soil infiltration rate is an important physical property measured as the speed of water with which it enters any soil, and it is highly dependent on soil texture (Liu et al., 2003). Soil infiltration rates can be measured with a ring infiltrometer (Moret-Ferna´ndez et al., 2012), and it is a measure of water retention capacity of soil. The soil type has a significant impact on water-holding capacity and infiltration rates (Bothma et al., 2012). Soil infiltration rates can be decreased by improving soil structures. Soil texture and clay contents also control soil’s water-holding capacity, which can help plants in the provision of water for some more duration compared to other soils. Soil organic matter has a great influence on soil physical attributes and thus controls its infiltration rate and water-holding capacity. All these soil factors together are responsible for the development of an integrated system based upon heterogeneity of soil physical features and control soil water-related properties (Gregory et al., 2006). 4.4.1.3 Plant mechanism to cope with drought 4.4.1.3.1 Signaling of stress

Under drought stress conditions, plant-signaling transduction is an important mechanism of intrabody communication. Plant roots have potential to sense variation in soil water contents (Davies et al., 2002) and can provide both chemical and hydraulic signals to plant shoot (Gollan et al., 1986). When plant roots experience drought or water stress, they provide stress signals to leaves in the form of variation in apoplast pH, cytokinin, malate, and many other factors involved in root shoot signaling transduction under drought stress (Schachtman and Goodger, 2008). Under drought, abscisic acid (ABA) production is upregulated in plants as it acts as a stress hormone that tend to mitigate stress (Zhang et al., 2006; Raghavendra et al., 2010). Apart from ABA, ROS play dual roles in plants, in which they act as suppressive factors on plant growth and sources of drought stress signal transduction in plants (Huang et al., 2012), which ultimately initiates the production of stress suppressing proteins such as phosphoprotein (Ke et al., 2009) and proline (Matysik et al., 2002) for molecular quenching of ROS.

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4.4.1.3.2 Growth and physiological modification

Drought imparts a severe impact on plant growth, such as reduction in seed germination (Kaya et al., 2006), less vegetative growth of plants (Manickavelu et al., 2006), and suppression of cell division and elongation (Hussain et al., 2008). Under drought stress, plant photosynthesis, stomatal conductance, and leaf growth are retarded (Manickavelu et al., 2006; Xu et al., 2010). Wild plants can induce flowering earlier in response to drought, whereas plants cropped by human needs to maintain yield as well, so they must adopt combating strategy to tolerate water deficiency without compromising on yield (Basu et al., 2016). In maintaining photosynthetic rate under water shortage, C4 plants have been adopted well compared to C3 plants with better water-use efficiency (Edwards and Walker, 1983). Combating with drought involves a complex interaction of metabolism, hormones (ABA), and ROS. If, under drought stress, genes such as ABI1 and ABI3 in plants are activated, ABI1 is upregulated and ABI3 is downregulated. The latter one is involved in drought stress tolerance in plants (Pinheiro and Chaves, 2011). Plant growth and physiological responses are under the influence of hormones (ABA, cytokinins, gibberellic acid, auxins, and ethylene) under such conditions (Wilkinson et al., 2012). Under drought stress, plant roots produce ABA, which is translocated to leaves for the closure of stomata (Wilkinson and Davies, 2010), but plants have to compromise on carbon assimilation (Ji et al., 2011), and in this aspect cytokinins can play an important role (Peleg et al., 2011). 4.4.1.3.3 Dehydration avoidance and tolerance

Plants when face dehydration tend either to avoid or tolerate it up to some extent. In dehydration avoidance, some hormonal and enzymatic modification results in leaf rolling (Kadioglu and Terzi, 2007) and the development of leaf cuticle layer to stop water loss form leaf surface (Ristic and Jenks, 2002). Leaf rolling in plant occurs due to the action of hormones and enzymes such as, soluble POD, ionically wall-bound POD, indole-3-acetic acid oxidase, polyphenol oxidase, and covalently wall-bound POD. Leaf lignification was positively correlated to the mentioned compounds and negatively related to nitrate reductase (Terzi et al., 2013). Thus under drought, plants either tend to escape drought or try to tolerate it. 4.4.1.3.4 Nutrient acquisition habits

Plant roots absorb nutrients and water from soil for plants depending on root architecture (Chapman et al., 2012), and drought severely affects plant nutrition acquisition habits. Among all nutrients, N is applied mostly as synthetic fertilizer, and nitrogen use efficiency (NUE) is of main concern regarding sustainable agriculture (Masclaux-Daubresse et al., 2010). Balanced nutrition (N, P, and K) application can mitigate adverse effects of water stress (Rhee et al., 2011), but water deficiency can lead to lower nutrient uptake as well. Nitrogen is very important for plant growth and development as it is a basic component of amino acids and biomolecules, but under drought, soil has less moisture impairment and lower uptake of N, and its increased volatilization losses (Silva et al., 2011). Under water stress, plants are unable to absorb much K and P leading to growth retardation, and biochemical processes slow down (Ge et al., 2012). Potassium is an essential element for

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plants mainly involved in plants’ osmotic balance and help plants withstand drought condition (Wang et al., 2013) and, if applied externally, can enhance the plant growth under water deficit conditions (Bahrami-Rad and Hajiboland, 2017). 4.4.1.3.5 Biochemical responses

Adaptive biochemical responses of plants under drought stress occur due to alteration in gene expression (Liu, 2003). Transgenic approaches have been used to monitor molecular changes in plants experiencing drought stress (Zhou et al., 2007), which ultimately has helped understanding plant drought responses (Yang et al., 2017a) because, in adaptive strategy, plants can accumulate proline and antioxidant enzymes to combat with drought stress (Yang et al., 2017a; Farooq et al., 2012). Besides these, plant cells can accumulate osmolytes such as glycine betaine, amino acids, organic acids, and polyols playing vital roles in biochemical functions of cells (Farooq et al., 2012). A study conducted on peach trees by Haider et al. (2018) has proved that peach tree leaves have shown biochemical changes such as accumulation of proline and sorbitol instead of sugars, and higher production of antioxidant enzymes upon exposure to drought. The accumulation of proteins and the activation of antioxidants (Yang et al., 2017a) are basic biochemical modification adopted by plants in response to drought stress. 4.4.1.3.6 Protein synthesis such as heat-shock proteins

Under water-stressed conditions, plants start accumulating heat-shock proteins (HSPs) (Hoekstra et al., 2001). They are also known as stress proteins present in almost every cell of every living organism (Li and Srivastava, 2004). The major role of HSPs is to maintain plant cells during the stress (Wang et al., 2003) and also to repair if any damage is already done to plant (Sato and Yokoya, 2007). Due to the activation of large set of genes (Wang et al., 2003), plants generally tend to produce these proteins under drought stress (Sato and Yokoya, 2007). Various studies have shown that these proteins are responsible for carrying out normal cellular processes (Wang et al., 2003) through protein production, proteins refolding (Sato and Yokoya, 2007). Moreover, they are also involved in reactivation of inactivated enzymes, stabilization of plant membranes (Marini et al., 2000; Sun et al., 2001), and developmental processes in plants, such as embryo and pollen development and fruit maturation (Wang et al., 2003). Although HSPs have five categories, but the most common one in plants is small HSP that ranges from 12 to 40 kDa in size (Wang et al., 2003). It has also been proved recently that HSPs act as antioxidizing agents for plants under shortage of water (Hamilton, 2001). 4.4.1.3.7 Antioxidant response

Antioxidant enzymes’ response of plants to drought is a defensive system that protects the plants from injuries due to active oxygen (Anjum et al., 2011) and ensures normal plant cell functioning (Horva´th et al., 2007). Basically under drought stress, the balance between production of ROS and activity of antioxidant enzymes in plants decides the scale of damage in plants (Møller et al., 2007). In order to fight with oxidative stress, plants also have nonenzymatic antioxidant protection system that regulates the strength of photosynthetic membranes in plants under water-deficient conditions (Anjum et al., 2011).

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The most common enzymatic and nonenzymatic antioxidants in plants that have scavenging effect on ROS species include SOD, catalase (CAT), and POD (Apel and Hirt, 2004). These antioxidants are known to have increased activities when the field capacity is as low as 25% (Apel and Hirt, 2004), especially for the complete destruction of singlet oxygen and peroxides in plant cells (Anjum et al., 2011). SOD has the ability to catalyze and dismutate O2 2 and convert it into H2O2, which is then scavenged by POD (Shigeoka et al., 2002). This is how these antioxidants induce resistance in plants against the oxidative stress of drought (Anjum et al., 2011). 4.4.1.3.8 Metabolic responses

Plant metabolism involves catabolism such as cellular respiration and anabolism such as photosynthesis, lipid and protein synthesis. Plant experiencing drought modifies or stops photosynthesis by closing stomata (Farooq et al., 2012). Besides carbohydrate metabolism (photosynthesis), lipid metabolism is also affected by drought and water stress. Lipids being integral and important part of cell membranes prevent compartmentation in cells under water stress. In A. thaliana, severe water-deficient lipids, such as monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), and phosphatidylcholines, were decreased linearly, and DGDG and MGDG increased. Upon rehydration, their amount increased as enzymatic assay shows that water-deficient deactivates enzymes responsible for the metabolism of these lipids (Gigon et al., 2004). This variation in lipid metabolism occurs due to fact that lipid unsaturation levels in plant tissue is high under water-deficient condition (Toumi et al., 2008). 4.4.1.3.9 Cellular responses

Stress signaling has been evolved in plant cells from energy sensing related cellular mechanisms involving ion/water homeostasis and production of stress-repressive proteins bringing cellular stability (Zhu, 2016). Cellular water contents, rate of loss of water, and drought stress level determine severity of plant stress response (Bray, 1997). Most common cellular organelles are peroxisomes (Hu et al., 2012); they alleviate abiotic stress experienced by plant cells (Smertenko, 2017). These small organelles play important roles such as ROS metabolism (Foyer and Noctor, 2003) and hormones production in cells (Hu et al., 2012) to mitigate drought stress. These small savers produce scavenger of excessive ROS (antioxidants ascorbate, SOD, glutathione, monodehydroascorbate reductase, APX CAT, SOD, and peroxiredoxins) to help plant cells mitigate oxidative damage under drought stress (Smertenko, 2017). Under drought conditions, pea plants have reported to produce higher SOD and APX (Mittler and Zilinskas, 1994), whereas drought-tolerant rice cultivar exhibits higher concentrations of these scavenger enzymes produced by peroxisomes (Guo et al., 2006). Mitochondria, another plant organelle, help cells modify cellular respiration upon the onset of drought making cellular energy balance possible (Atkin and Macherel, 2009). Combined action of these cellular organelles and other metabolic responses are vital for drought tolerance under drought stress. 4.4.1.3.10 Gene induction and expression

Drought stress directly affects plant growth and seed production rate (Shinozaki et al., 2003). Many plants respond to such conditions at transcriptional level to generate products

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that work in plant drought stress response (Alter et al., 2015). There are two major groups of genes that produce their independent responses during drought stress (Shinozaki et al., 2003). One group produces products to save plants from stress, whereas the other group produces signals in response to stress (Shinozaki et al., 2003). Plants also undergo transcription responses to drought stress that involve many cis/trans-acting factors (Shinozaki et al., 2003). According to scientists, there are ABA involvements in plant gene response toward water deficit (Zhu et al., 2001). Transcriptomics data have clearly shown the involvement of mRNA response to drought stress (Priyanka et al., 2010; Rasmussen et al., 2013). Data have also shown the coexpression of genes and proteins under such conditions (Zandalinas et al., 2018). 4.4.1.3.11 Organelle response

During drought stress, plants fail to keep the balance of ROS in their cells and fulfill the antioxidant requirement in plant cells (Hossain et al., 2012). This leads to extreme damages of proteins, lipids, and nucleic acid molecules present in plant cells (Rinalducci et al., 2008). To counter this stress, plants have very well-developed defense system that involves both enzymatic and nonenzymatic mechanisms (Hossain et al., 2010). The cellular system aids these mechanisms by sending different stress signals to cell organelles (Desikan et al., 2001). As the stress signals reach cell surfaces, they produce their response at the outer surface first and then activate the responsive mechanism inside of plants (Huang et al., 2012). Actually the presence of ROS is the stress signal that activates plant cell defensive mechanism is the primary stress response of plants (Agrawal et al., 2011). Moreover, proteins receptors are also present in the cell membrane, which immediately respond to stress signals (Komatsu et al., 2007).

4.4.2 Exogenous amendments for combating drought A basic concept is that current human activities are not in line with sustainable development concepts. Water resources are being depleted, and soils are lacking nutrients necessary for plant growth and being degraded by erosion due to extensive tillage. Due to unavailability of water, crops are facing stresses and human, facing food security. The problem of water scarcity is not easily solved. So, the other methods such as application of organic and inorganic amendments such as biosolids, pulp and paper industry waste, livestock manure, crop residues, calcium carbonate, zeolite, and gypsum can enhance waterholding capacity of soil and may also improve soil properties. The organic amendments, which are readily decomposable, can provide immediate but temporary solution, whereas stable organic amendments can provide long-lasting effects (Larney and Angers, 2012). 4.4.2.1 Organic amendments Organic amendments include an addition of a composted organic residue in soil, which can enhance plant growth, provide nutrients for uptake, enhance mycorrhizal colonization, increase SOD contents and total POD activities in plant shoots. An addition of compost significantly increases the plant growth, foliar nutrients (N, P, and K), and tissue water content of the plants during drought. Peroxidases (POX) activity in plants increases during

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drought up to 250 %. Drought decreased the SOD but by adding crop residues (Rolda´n et al., 2008). An addition of sewage sludge decreased microbial respiration and increased organic matter in soil, which ultimately improved soil properties and plant growth (Pascual et al., 2004; Medina and Azco´n, 2010). Organic amendments not only help soil retain more water but also improve soil physical and chemical properties such as enhancing soil organic matter, which is helpful in increasing population and activity of the soil indigenous microbial biomass (Hueso et al., 2012). A long-lasting application of organic amendments in drought-affected soils resulted in increased organic carbon by up to 90% and better coping with drought stress. But, regular addition is required till the complete eradication of drought stress symptoms as the increase in crop yield is recorded up to 250% by this practice (Diacono and Montemurro, 2010). A soil incubation experiment was carried out to assess the impact of drought and organic amendments roles for recovery and was concluded that organic amendments restore the native microbial communities in the drought-affected soil. Thus physical, chemical, and biochemical parameters of soil were recovered (Hueso et al., 2011). 4.4.2.2 Inorganic amendments Various inorganic amendments have been identified, which play a significant role in rehabilitation of stressed soil and plants and improve the chemical and physical properties. Sand, peat, and zeolite were added to the drought-stressed soil, and it was concluded that an addition of inorganic amendments improves the physical and chemical properties of the soil (Ok et al., 2003). Amended soil with sand contained creates spaces for aeration, and these spaces help in proper aeration and water usage during drought (Miller, 2000). Sand also increases plant-available water (Curtis and Claassen, 2008). Inorganic amendments improve water and nutrient retention of root zones in terms of CEC, selectivity of potassium (K) versus calcium (Ca) on exchange sites, and nutrient leaching (McCoy and Stehouwer, 1999). Calcined clay, diatomaceous earth, zeolite, and crystalline SiO2 significantly improve water-holding ability, soil strength, bulk density, and oxygen diffusion rate in drought stress (Wehtje et al., 2003).

4.4.3 Microbe plant interactions One of the major challenges of the 21st century is the production of sufficient food for human that is expected to reach 10 billion by 2050. It means that we will have to increase agricultural productivity. But agriculture in different areas is facing a wide range of problems such as depletion of water resources without which agricultural production cannot be increased. Therefore different measures are being adopted for this purpose. The use of microbes for nitrogen fixation and plant growth has been well known. They also provide help in mitigating different stresses that a plant is facing by providing disease resistance and aid in nutrient availability and uptake (Morrissey et al., 2004). Root-colonizing bacteria can increase plant resistance against drought stress factors when they are applied as biofertilizers. Root-endogenous bacteria can increase plants tolerance against all abiotic stresses such as drought, salinity, and metal toxicity providing the opportunity and effective method to control all types of abiotic disease resistance and

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control (Dimkpa et al., 2009). Bactria living in rhizosphere also help in alleviating drought tolerance in plants. Three strains of bacteria are efficient in this regard, including Pseudomonas putida, Pseudomonas sp., and Bacillus megaterium, as they have developed mechanisms to help plants cope with drought stress. They increase in indole acetic acid (IAA) production and induce resistance to drought in plants. They also increase shoot, root biomass, and plant tissue water content under drought conditions (Marulanda et al., 2009). Microbes also improve nutrient acquisition and stimulate hormones and control drought effects and consequences (Berg, 2009). PGPR make colonies at the rhizosphere of plants and increase plant growth, reduce disease susceptibility, and produce “induced systemic tolerance” in response coping with drought stress. It can also increase nutrient uptake, thus reducing the requirement of fertilizers and prevents the accumulation of nitrates and phosphates in soils (Yang et al., 2009). 4.4.3.1 Plant growth promoting rhizobacteria Out of many possible ways of drought stress amelioration one is delay in leaf flowering, PGPR induce a delay in flowering time, which causes increased biomass yield (Bresson et al., 2013). The application of PGPR in water stress conditions improves the antioxidant and photosynthetic pigments in basil plants and increased the CAT enzyme activity (Heidari and Golpayegani, 2012). The bacteria classified under PGPR help increase crop yield productivity and can provide drought-stress resistance. A wide range of rootcolonizing bacteria have been classified under PGPR class, which can produce a wide range of enzymes and metabolites helpful to plants for coping with drought stress (Ngumbi and Kloepper, 2016). Priming of plant roots by microorganisms can also induce resistance against drought after conditioning treatment (Beckers and Conrath, 2007). Sandhya et al. (2010) used PGPR strains against drought-stressed plants. The results showed that inoculated plants produced high proline, sugars, and amino acids under drought stress. It also decreased electrolyte leakage, decreased antioxidant enzymes (APX), CAT, glutathione POD production showing that seedlings inoculated with PGPR felt less stress as compared to uninoculated seedlings in maize. Under drought stress conditions, ethylene production increase can affect plant roots, but PGPR contain a vital enzyme, ACC deaminase, which regulates ethylene production by metabolizing ACC into α-ketobutyrate and ammonia and prevents plant injury or death (Saleem et al., 2007). Arshad et al. (2008) selected two PGPR inoculums and investigated their potential to reduce the drought effect on growth, yield, and ripening of pea (Pisum sativum L.). Results showed that PGPR decreased the drought stress and increased the growth and yield of peas. Drought stress at the vegetative growth stage decreased shoot growth by 41% in the absence of PGPR, and by using PGPR, only 18% reduction in yield was recorded. The same case was seen in grain yield and PGPR inoculums resulted in 40% 62% higher grain yield. One of the other mechanisms by which PGPR can enhance plant growth and alleviate drought stress is the production of plant hormone such as cytokinin. Plants facing drought stress had higher relative water content and leaf water potential compared with those of noninoculated ones. Water supply levels, the root exudates, sugars, amino acids, and organic acids were increased because of PGPR inoculation. Initially, drought stress reduced the shoot cytokinin concentration by 39.14%, but adding PGPR lowered this

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value to 10.22%. Stomatal conductance also increased showing that PGPR can perform well as a drought stress inhibitor (Liu et al., 2013). In addition to these, soils inoculated with PGPR have higher dehydrogenase and phosphatase activities than the normal soil (Kohler et al., 2009). 4.4.3.1.1 Phytohormone production

Phytohormones levels become irregular according to the severity of drought as the amount of IAA decreased up to the three times more than the normal and gibberellic acid level that changed irregularly during stress period; ABA amounts also increased (Nihal et al., 2009). Progressive drought generally has effects on leaf growth, rate of photosynthesis, and phytohormone contents as a decline in cytokinin contents, rather than ABA accumulation, because ABA accumulated when the growth has been already suppressed (Pustovoitova et al., 2003). During stress, leaf senescence (a physiological process) contributes to nutrient remobilization from leaves of plant to other with the help of salicylic acid and jasmonic acid, allowing the rest of the plant to benefit from the nutrients accumulated in the leaf with the help of the. Salicylic acid concentration rises up to 80%, and jasmonic acid levels decrease by 40% allowed senescence. It is therefore can be said that salicylic acid application can help in the regulation of drought stress by inducing leaf senescence (Abreu and Munne´-Bosch, 2008). ABA and ethylene play an important role in plants to adapt under drought stress as these hormones can cause morphological, physiological, and chemical changes in plants and ensure plant survival under water stress. ABA can induce stomata closure; thus reduction in transpiration occurs. It also can reduce leaf surface area, increase the root: shoot ratio, and support to uptake plant water from soil as by decreasing plant tissue water potential compared to water-deficient environment by osmotic adjustment. IAA increases root exudation, which can directly and/or indirectly increase phosphorus mobilization in soil (Wittenmayer and Merbach, 2005). Although jasmonic acid, cytokinins, and ethylene are also involved in controlling stomatal conductance, ABA is the best known stress phytohormone that closes the stomata under water deficit. Its interaction with jasmonic acid and nitric oxide can increase its potential of closing stomatal conductance. In addition to all these, ABA is involved in gene activation and signaling responsible for the production of other phytohormones such as ethylene, auxin, and cytokinin (DaszkowskaGolec and Szarejko, 2013; Li et al., 2014). Phytohormones increase photosynthetic rate during drought stress; increased phytic acid levels and phytohormone organization patterns show their importance in controlling hormonal regulation and plant growth and development in drought stress conditions (Georges et al., 2009; De Diego et al., 2012). 4.4.3.1.2 Root growth modification

Drought stress has effects on the synthesis and distribution of plant growth regulators with some emphasis on ABA production, which plays a growth regulator in stress conditions and reduction in root tip turgor. In stress conditions, ABA will reduce the synthesis and transport of cytokinins in the root tip that reduces transport (Wilkinson and Davies, 2010). Results indicate that root growth in drought stress significantly increases in search of water to cope with drought (Cairns et al., 2004). In drought stress, plants tend to increase the root:shoot biomass ratio as it elongates its primary root, root branching, and

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root biomass up to 60% to help plants absorb more water. Cytokinin that is a hormone and is involved in the regulation of root growth plays a vital role in increasing the root: shoot biomass ratio. To cope with drought stress, plants need to do osmotic adjustments, modification in root growth, accumulation of low- and high-molecular-weight solutes, and water-soluble sugars (Jiang and Huang, 2001). 4.4.3.1.3 Osmolytes accumulation in plant tissue

Osmolytes benefit plants under drought conditions by sustaining cell and tissue activities and induce an effective tolerance. One tolerance mechanism identified is the maintenance of root development to reach water that may be available deeper in the soil profile (Serraj and Sinclair, 2002). Many plants accumulate osmolytes in response to the imposition of environmental stresses that cause drought. Osmolytes such as proline and glycine betaine synthesis buffer the cellular redox potential (Hare et al., 1998). Malondialdehyde concentration and Na1, K1, proline, and soluble sugars also increase in drought stress plants (Yousfi et al., 2010). Under drought, plants tend to increase the Na-to-K ratio, which can be dangerous for plants and must be coped with. Potassium fertilizer application can be a solution to this. Water stress triggers the production of proline and glucose in plants, leaves, and tap roots, but under long-lasting drought condition, the activation of effective mechanism of osmotic adjustment in shoot and root of plant is critical and crucial for plant survival (Choluj et al., 2008). 4.4.3.1.4 Drought tolerance gene induction in plants

Gene expressions during drought stress helps in alleviating drought and improving plant growth. During the production of this expression, dehydration-responsive elementbinding protein 1A (DREB1A), a transcription factor interacts with dehydration-responsive element (DRE) and produces tolerance of drought stress (Kasuga et al., 1999). Final product (proteins/enzymes) produced by stress inducible genes can function in initial and advanced stages of stress thus help plants in stress tolerance (Shinozaki et al., 2003). Advanced molecular and genomic studies have reported that multifunctional genes can be induced by cold and drought stress as various transcription factors regulate them. The final product of these genes not only mitigates stress in plants but also acts as stress signal in plants at cellular level as identified by various genetic studies (Shinozaki and Yamaguchi-Shinozaki, 2007). As described earlier, ABA involved in plants’ drought stress mitigation is produced in response to drought stress and induces NCED gene of Arabidopsis. Similarly, AtNCED3 is induced and controls endogenous stress condition (Iuchi et al., 1996). Work done by Taji et al. (2002) has screened such stress-responsive genes (AtGolS1, 2, and 3), which offer promising results in galactinol and raffinose accumulation acting as osmo-protectants under drought stress conditions. 4.4.3.2 Mycorrhizal association In drought conditions, plants can interact with fungi to fight with drought. Plants association with fungi is called mycorrhizal. As drought stress least effect the mycorrhizal colonization, the survival chances of plants under drought stress increase. Water potential also increases in mycorrhizal plants by 26% in combination with improvements up to 92%

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in transpiration, 45% stomatal conductance, and 88% net photosynthesis (Morte et al., 2000). According to Khalvati et al. (2009), roots associated with mycorrhizae cause decrease in oxidative damage to rhizosphere, increase in enzyme activities, reduction in drought stress, and improve tolerance to drought stress (Subramanian and Charest, 1999; Levy et al., 1983). For example, when maize plants were exposed to drought stress for 3 weeks, enzyme activities increased in plants associated with mycorrhizal fungi. Total amino acids concentrations were also recorded 56% 75% higher (Subramanian et al., 1995).

4.4.4 Genetic engineering of drought-tolerant crops For sustainable crop production, it is required that the plants can tolerate drought stress, and it is crucial for agricultural production worldwide. Recent progresses have been made, which advance our understanding of gene expression, signal transduction, and transcriptional regulation in plants experiencing drought (Umezawa et al., 2006). Drought stress tolerant plants’ genetic engineering requires a basic understanding of plant’s physiological, biochemical, and gene regulation network. Genetic make up of few crops make them drought tolerant like Populus kangdingensis (Yang and Miao, 2010). Modern day CRISPR techniques are promising approaches for selection, cutting and interspecie transfer/ insertion of drought stress mitigating gene. Research conducted by Li et al. (2019) has show that SlNPR1 is gene associated with drought tolerance in tomato plants. Inter specie transfer, up regulation and down regulation is promising approach in genetic engineering of drought tolerant plant as gene editing with CRISPR/Cas9 has huge potential for crop improvement (Chilcoat et al., 2017).

4.5 Salient features of drought-tolerant plants Natural drought-tolerant plants can prove valuable to assess the drought-tolerance capacity. A. thaliana can withstand water deficit better than many other plants (Bartels and Sunkar, 2005). Plants that overexpress the vacuolar H1 pyrophosphatase have more resistance against drought because they accumulate more Na1 and K1 ions in their leaf tissues; the uptake of cations from vesicles is enhanced. This enhanced uptake results in the increase in solute accumulation and water retention. In addition, cation sequestration can also reduce drought effects (Gaxiola et al., 2001).

4.6 Summary Drought is a worldwide problem, and recent climate change has been making it worse. Drought causes severe economic losses to agriculture and ultimately affects human food chain. Crop plants under drought stress produce low yield, but in extreme drought, plants may die. To combat with drought, plants adopt molecular, physiological, nutritional, and

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metabolic modifications. The exogenous application of amendments may also help plants withstand drought stress and produce significant yield. Plants’ natural adaptation along with breeding and biotechnological plant engineering can help them engineer droughttolerant plant species for sustainable agriculture of changing the present international scenario.

References Abreu, M.E., Munne´-Bosch, S., 2008. Salicylic acid may be involved in the regulation of drought-induced leaf senescence in perennials: a case study in field-grown Salvia officinalis L. plants. Environ. Exp. Bot. 64, 105 112. Adams, H.D., Guardiola-Claramonte, M., Barron-Gafford, G.A., Villegas, J.C., Breshears, D.D., Zou, C.B., et al., 2009. Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proc. Natl. Acad. Sci. U.S.A. 106, 7063 7066. Agrawal, G.K., Bourguignon, J., Rolland, N., Ephritikhine, G., Ferro, M., Jaquinod, M., et al., 2011. Plant organelle proteomics: collaborating for optimal cell function. Mass Spectrom. Rev. 30, 772 853. Andreadis, K.M., Lettenmaier, D.P., 2006. Trends in 20th century drought over the continental United States. Geophys. Res. Lett. 33. Anjum, S., Xie, X., Wang, L., 2011. Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agric. Res. 6 (9), 2026 2032. Alter, S., Bader, K.C., Spannagl, M., Wang, Y., Bauer, E., Scho¨n, C.C., et al., 2015. Drought DB: an expert-curated compilation of plant drought stress genes and their homologs in nine species. Database 2015, bav046. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373 399. Aranjuelo, I., Molero, G., Erice, G., Avice, J.C., Nogue´s, S., 2010. Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.). J. Exp. Bot. 62, 111 123. Armada, E., Rolda´n, A., Azcon, R., 2014. Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and salvia plants species under drought conditions in natural arid soil. Microb. Ecol. 67, 410 420. Arshad, M., Shaharoona, B., Mahmood, T., 2008. Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.). Pedosphere 18, 611 620. Ashraf, M., Harris, P.J.C., 2013. Photosynthesis under stressful environments: an overview. Photosynthetica 51, 163 190. Aslam, M., Zamir, I., Afzal, I., Yaseen, M., Mubeen, M., Shoaib, A., 2013. Drought tolerance in maize through Potassium: drought stress, its effect on maize production and development of drought tolerance through potassium application. Cercet. Agron. Mold. XLVI, 16. Asner, G.P., Alencar, A., 2010. Drought impacts on the Amazon forest: the remote sensing perspective. New Phytol. 187 (3), 569 578. Atkin, O.K., Macherel, D., 2009. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot. 103, 581 597. Bahrami-Rad, S., Hajiboland, R., 2017. Effect of potassium application in drought-stressed tobacco (Nicotiana rustica L.) plants: comparison of root with foliar application. Ann. Agric. Sci. 62, 121 130. Balestrini, R., Lumini, E., Borriello, R., Bianciotto, V., 2015. Plant-soil biota interactions. Soil Microbiology, Ecology and Biochemistry. pp. 311 338. Barbeta, A., Mejı´a-Chang, M., Ogaya, R., Voltas, J., Dawson, T.E., Pen˜uelas, J., 2015. The combined effects of a long-term experimental drought and an extreme drought on the use of plant-water sources in a Mediterranean forest. Global Change Biol. 21, 1213 1225. Bartels, D., Sunkar, R., 2005. Drought and salt tolerance in plants. CRC Crit. Rev. Plant Sci. 24, 23 58. Basu, S., Ramegowda, V., Kumar, A., Pereira, A., 2016. Plant adaptation to drought stress. F1000Research 5, 1554. Beckers, G.J., Conrath, U., 2007. Priming for stress resistance: from the lab to the field. Curr. Opin. Plant Biol. 10, 425 431. Benson, C., Clay, E., 1994. The impact of drought on sub-Saharan African economies. IDS Bull. 25, 24 32.

Plant Life under Changing Environment

96

4. Regulation of drought stress in plants

Berg, G., 2009. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol. 84, 11 18. Berg, A., Lintner, B.R., Findell, K.L., Malyshev, S., Loikith, P.C., Gentine, P., 2014. Impact of soil moistureatmosphere interactions on surface temperature distribution. J. Clim. 27, 7976 7993. Berland, A., Shiflett, S.A., Shuster, W.D., Garmestani, A.S., Goddard, H.C., Herrmann, D.L., et al., 2017. The role of trees in urban stormwater management. Landsc. Urban Plan. 162, 167 177. Berry, J.A., Beerling, D.J., Franks, P.J., 2010. Stomata: key players in the earth system, past and present. Curr. Opin. Plant Biol. 13, 233 240. Bothma, C.B., van Rensburg, L.D., le Roux, P.A.L., 2012. Rainfall intensity and soil physical properties influence on infiltration and runoff under in-field rainwater harvesting conditions. Irrig. Drain. 61, 41 49. Boyer, J.S., 2015. Turgor and the transport of CO2 and water across the cuticle (epidermis) of leaves. J. Exp. Bot. 66, 2625 2633. Bray, E., 1997. Plant responses to water deficit. Trends Plant Sci. 2, 48 54. Breshears, D.D., Knapp, A.K., Law, D.J., Smith, M.D., Twidwell, D., Wonkka, C.L., 2016. Rangeland responses to predicted increases in drought extremity. Rangelands 38, 191 196. Bresson, J., Varoquaux, F., Bontpart, T., Touraine, B., Vile, D., 2013. The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytol. 200, 558 569. Cairns, J.E., Audebert, a, Townend, J., Price, A.H., Mullins, C.E., 2004. Effect of soil mechanical impedance on root growth of two rice varieties under field drought stress. Plant Soil 267, 309 318. Calow, R.C., MacDonald, A.M., Nicol, A.L., Robins, N.S., 2010. Ground water security and drought in Africa: linking availability, access, and demand. Ground Water 48, 246 256. Carolina, N., Branch, M., Division, S.S., Climatic, N., 2002. Century drought indices used in the United States. Bull. Am. Meteorol. Soc. 22, 1149 1165. Chai, Q., Gan, Y., Zhao, C., Xu, H.L., Waskom, R.M., Niu, Y., et al., 2016. Regulated deficit irrigation for crop production under drought stress. A review. Agron. Sustain. Dev. 36, 1 21. Chapman, N., Miller, A.J., Lindsey, K., Whalley, W.R., 2012. Roots, water, and nutrient acquisition: let’s get physical. Trends Plant Sci. 17, 701 710. Chilcoat, D., Liu, Z.B., Sander, J., 2017. Use of CRISPR/Cas9 for crop improvement in maize and soybean. In: Progress in Molecular Biology and Translational Science. vol. 149. Academic Press, pp. 27 46. Choluj, D., Karwowska, R., Ciszewska, A., Jasinska, M., 2008. Influence of long-term drought stress on osmolyte accumulation in sugar beet (Beta vulgaris L.) plants. Acta Physiol. Plant. 30, 679 687. Ciais, P., Reichstein, M., Viovy, N., Granier, A., Oge´e, J., Allard, V., et al., 2005. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529 533. Cook, E.R., Seager, R., Cane, M.A., Stahle, D.W., 2007. North American drought: reconstructions, causes, and consequences. Earth-Sci. Rev. 81, 93 134. Chaves, M.M., Flexas, J., Pinheiro, C., 2009. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot. 103 (4), 551 560. Curtis, M.J., Claassen, V.P., 2008. An alternative method for measuring plant available water in inorganic amendments. Crop Sci. 48 (6), 2447 2452. ˆ .C., Ahnert, D., Baligar, V.C., 2017. Influence of low light da Silva Branco, M.C., de Almeida, A.A.F., Dalmolin, A intensity and soil flooding on cacao physiology. Sci. Hortic. (Amsterdam). 217, 243 257. Daszkowska-Golec, A., Szarejko, I., 2013. Open or close the gate stomata action under the control of phytohormones in drought stress conditions. Front. Plant Sci. 4, 138. Davies, W.J., Wilkinson, S., Loveys, B., 2002. Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytol. 153, 449 460. De Diego, N., Pe´rez-Alfocea, F., Cantero, E., Lacuesta, M., Moncalea´n, P., 2012. Physiological response to drought in radiata pine: phytohormone implication at leaf level. Tree Physiol. 32, 435 449. de Souza, A.P., Cocuron, J.-C., Garcia, A.C., Alonso, A.P., Buckeridge, M.S., 2015. Changes in whole-plant metabolism during grain-filling stage in Sorghum bicolor L. (Moench) grown under elevated CO2 and drought. Plant Physiol. 2015, 01054. Desikan, R., Soheila, A.H., Hancock, J.T., Neill, S.J., 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127 (1), 159 172.

Plant Life under Changing Environment

References

97

Diacono, M., Montemurro, F., 2010. Long-term effects of organic amendments on soil fertility. A review. Agron. Sustain. Dev. 30, 401 422. Dimkpa, C., Weinand, T., Asch, F., 2009. Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 32, 1682 1694. Duran-Encalada, J.A., Paucar-Caceres, A., Bandala, E.R., Wright, G.H., 2017. The impact of global climate change on water quantity and quality: a system dynamics approach to the US Mexican transborder region. Eur. J. Oper. Res. 256, 567 581. Edwards, G., Walker, D.A., 1983. C3, C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis. p. 542. Univ of California Press. Elliott, J., Deryng, D., Mu¨ller, C., Frieler, K., Konzmann, M., Gerten, D., et al., 2014. Constraints and potentials of future irrigation water availability on agricultural production under climate change. Proc. Natl. Acad. Sci. U.S.A. 111, 3239 3244. Fang, X., Pomeroy, J.W., 2008. Drought impacts on Canadian prairie wetland snow hydrology. Hydrol. Process. 22, 2858 2873. Fang, Y., Xiong, L., 2015. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell. Mol. Life Sci. 72, 673 689. FAO, 2014. Drought. FAO L. Water 1 4. Faraloni, C., Cutino, I., Petruccelli, R., Leva, A.R., Lazzeri, S., Torzillo, G., 2011. Chlorophyll fluorescence technique as a rapid tool for in vitro screening of olive cultivars (Olea europaea L.) tolerant to drought stress. Environ. Exp. Bot. 73, 49 56. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S.M.A., 2009. Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29, 185 212. Farooq, M., Hussain, M., Wahid, A., Siddique, K.H.M., 2012. Drought stress in plants: an overview. Plant Responses to Drought Stress. Springer, Berlin, Heidelberg, 1 33. Fathi, A., Tari, D.B., 2016. Effect of drought stress and its mechanism in plants. Int. J. Life Sci. 10, 1. Flexas, J., Medrano, H., 2002. Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann. Bot. 89, 183 189. Flexas, J., Bota, J., Loreto, F., Cornic, G., Sharkey, T.D., 2004. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol. 6, 269 279. Foyer, C.H., Noctor, G., 2003. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant. 119, 355 364. Gaxiola, R.A., Li, J., Undurraga, S., Dang, L.M., Allen, G.J., Alper, S.L., et al., 2001. Drought- and salttolerant plants result from overexpression of the AVP1 H 1 -pump. Proc. Natl. Acad. Sci. U.S.A. 98, 11444 11449. Ge, T.-D., Sun, N.-B., Bai, L.-P., Tong, C.-L., Sui, F.-G., 2012. Effects of drought stress on phosphorus and potassium uptake dynamics in summer maize (Zea mays) throughout the growth cycle. Acta Physiol. Plant. 34, 2179 2186. Georges, F., Das, S., Ray, H., Bock, C., Nokhrina, K., Kolla, V.A., et al., 2009. Over-expression of Brassica napus phosphatidylinositol-phospholipase C2 in canola induces significant changes in gene expression and phytohormone distribution patterns, enhances drought tolerance and promotes early flowering and maturation. Plant Cell Environ. 32, 1664 1681. Gigon, A., Matos, A.R., Laffray, D., Zuily-Fodil, Y., Pham-Thi, A.T., 2004. Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (Ecotype Columbia). Ann. Bot. 94, 345 351. Gollan, T., Passioura, J.B., Munns, R., 1986. Soil water status affects the stomatal conductance of fully turgid wheat and sunflower leaves. Aust. J. Plant Physiol. 13, 459 464. Greenwood, S., Ruiz-Benito, P., Martı´nez-Vilalta, J., Lloret, F., Kitzberger, T., Allen, C.D., et al., 2017. Tree mortality across biomes is promoted by drought intensity, lower wood density and higher specific leaf area. Ecol. Lett. 20, 539 553. Gregory, J., Dukes, M., Jones, P., Miller, G., 2006. Effect of urban soil compaction on infiltration rate. J. Soil Water Conserv. 61, 117 124. Guo, Z., Ou, W., Lu, S., Zhong, Q., 2006. Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol. Biochem. 44, 828 836. Gurmu, E., Mace, R., 2008. Fertility decline driven by poverty: the case of Addis Ababa, Ethiopia. J. Biosoc. Sci. 40, 339 358.

Plant Life under Changing Environment

98

4. Regulation of drought stress in plants

Haider, M.S., Kurjogi, M.M., Khalil-ur-Rehman, M., Pervez, T., Songtao, J., Fiaz, M., et al., 2018. Drought stress revealed physiological, biochemical and gene-expressional variations in ‘Yoshihime’ peach (Prunus Persica L) cultivar. J. Plant Interact. 13, 83 90. Hamilton, E.W., 2001. Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126, 1266 1274. Hao, Z., Singh, V.P., 2015. Drought characterization from a multivariate perspective: a review. J. Hydrol 527, 668 678. Hare, P.D., Cress, W.A., Van Staden, J., 1998. Dissecting the roles of osmolyte accumulation during stress. Plant, Cell Environ. 21, 535 553. Hasibeder, R., Fuchslueger, L., Richter, A., Bahn, M., 2015. Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol. 205, 1117 1127. Heidari, M., Golpayegani, A., 2012. Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). J. Saudi Soc. Agric. Sci. 11, 57 61. Helman, D., Lensky, I.M., Yakir, D., Osem, Y., 2017. Forests growing under dry conditions have higher hydrological resilience to drought than do more humid forests. Global Change Biol. 23, 2801 2817. Hoekstra, F.A., Golovina, E.A., Buitink, J., 2001. Mechanisms of plant desiccation tolerance. Trends Plant Sci. 6, 431 438. Hossain, M.A., Cho, J.I., Han, M., Ahn, C.H., Jeon, J.S., An, G., et al., 2010. The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J. Plant Physiol. 167 (17), 1512 1520. Hossain, Z., Nouri, M.Z., Komatsu, S., 2012. Plant cell organelle proteomics in response to abiotic stress. J. Proteome Res. 11 (1), 37 48. Horva´th, E., Pa´l, M., Szalai, G., Pa´ldi, E., Janda, T., 2007. Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. Biol. Plant. 51 (3), 480 487. Hu, J., Baker, A., Bartel, B., Linka, N., Mullen, R.T., Reumann, S., et al., 2012. Plant peroxisomes: biogenesis and function. Plant Cell 24, 2279 2303. Huang, G.T., Ma, S.L., Bai, L.P., Zhang, L., Ma, H., Jia, P., et al., 2012. Signal transduction during cold, salt, and drought stresses in plants. Mol. Biol. Rep. 39 (2), 969 987. Hueso, S., Herna´ndez, T., Garcı´a, C., 2011. Resistance and resilience of the soil microbial biomass to severe drought in semiarid soils: the importance of organic amendments. Appl. Soil Ecol. 50, 27 36. Hueso, S., Garcı´a, C., Herna´ndez, T., 2012. Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils. Soil Biol. Biochem. 50, 167 173. Hussain, M., Malik, M.A., Farooq, M., Ashraf, M.Y., Cheema, M.A., 2008. Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. J. Agron. Crop Sci. 194, 193 199. IEA, 2015. Energy and Climate Change. World Energy Outlook Special Reports. pp. 1 200. Iizumi, T., Ramankutty, N., 2015. How do weather and climate influence cropping area and intensity? Global Food Sec. 4, 46 50. Iovieno, P., Punzo, P., Guida, G., Mistretta, C., Van Oosten, M.J., Nurcato, R., et al., 2016. Transcriptomic changes drive physiological responses to progressive drought stress and rehydration in tomato. Front. Plant Sci. 7, 371. Iuchi, S., Yamaguchi-Shinozaki, K., Urao, T., Terao, T., Shinozaki, K., 1996. Novel drought-inducible genes in the highly drought-tolerant cowpea: cloning of cDNAs and analysis of the expression of the corresponding genes. Plant Cell Physiol. 37, 1073 1082. Ji, X., Dong, B., Shiran, B., Talbot, M.J., Edlington, J.E., Hughes, T., et al., 2011. Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiol. 156, 647 662. Jiang, Y., Huang, B., 2001. Osmotic adjustment and root growth associated with drought preconditioningenhanced heat tolerance in Kentucky bluegrass. Crop Sci. 41, 1168 1173. Kadioglu, A., Terzi, R., 2007. A dehydration avoidance mechanism: leaf rolling. Bot. Rev. 73, 290 302. Kang, Y., Khan, S., Ma, X., 2009. Climate change impacts on crop yield, crop water productivity and food security—a review. Prog. Nat. Sci. 19, 1665 1674. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K., 1999. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17, 287 291.

Plant Life under Changing Environment

References

99

Kay, R.N.B., 1997. Responses of African livestock and wild herbivores to drought. J. Arid Environ. 37, 683 694. ¨ ., 2006. Seed treatments to overcome salt and drought stress Kaya, M.D., Okc¸u, G., Atak, M., C ¸ ikili, Y., Kolsarici, O during germination in sunflower (Helianthus annuus L.). Eur. J. Agron. 24, 291 295. Ke, Y., Han, G., He, H., Li, J., 2009. Differential regulation of proteins and phosphoproteins in rice under drought stress. Biochem. Biophys. Res. Commun. 379, 133 138. Khalvati, M., Bartha, B., Dupigny, A., Schro¨der, P., 2009. Arbuscular mycorrhizal association is beneficial for growth and detoxification of xenobiotics of barley under drought stress. J. Soils Sediments 10, 54 64. Kohler, J., Caravaca, F., Rolda´n, A., 2009. Effect of drought on the stability of rhizosphere soil aggregates of Lactuca sativa grown in a degraded soil inoculated with PGPR and AM fungi. Appl. Soil Ecol. 42, 160 165. Kolb, T., Dore, S., Montes-Helu, M., 2013. Extreme late-summer drought causes neutral annual carbon balance in southwestern ponderosa pine forests and grasslands. Environ. Res. Lett. 8, 15015. Komatsu, S., Konishi, H., Hashimoto, M., 2007. The proteomics of plant cell membranes. J. Exp. Bot. 58 (1), 103 112. Larney, F.J., Angers, D.A., 2012. The role of organic amendments in soil reclamation: a review. Can. J. Soil Sci. 92, 19 38. Lesk, C., Rowhani, P., Ramankutty, N., 2016. Influence of extreme weather disasters on global crop production. Nature 529, 84 87. Levine, L., 2013. The increase in unemployment since 2007: is it cyclical or structural? Congr. Res. Serv. 15, 1 17. Levy, Y., Syvertsen, J.P., Nemec, S., 1983. Effect of drought stress and vesicular arbuscular mycorrhiza on citrus transpiration and hydraulic conductivity of roots. New Phytol. 93, 61 66. Li, R., Liu, C., Zhao, R., Wang, L., Chen, L., Yu, W., et al., 2019. CRISPR/Cas9-Mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol. 19, 38. Li, Z., Srivastava, P., 2004. Heat-shock proteins. Curr. Protoc. Immunol. Available from: https://doi.org/ 10.1002/0471142735.ima01ts58. Li, Z., Zhou, H., Peng, Y., Zhang, X., Ma, X., Huang, L., et al., 2014. Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. Plant Growth Regul. 76, 71 82. Li, Y., Li, H., Li, Y., Zhang, S., 2017. Improving water-use efficiency by decreasing stomatal conductance and transpiration rate to maintain higher ear photosynthetic rate in drought-resistant wheat. Crop J. 5, 231 239. Lim, J.H., Kim, S.D., 2013. Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol. J. 29, 201 208. Lin, Y., Deng, X., Jin, Q., 2013. Economic effects of drought on agriculture in North China. Int. J. Disaster Risk Sci. 4, 59 67. Lipiec, J., Doussan, C., Nosalewicz, A., Kondracka, K., 2013. Effect of drought and heat stresses on plant growth and yield: a review. Int. Agrophysics 27 (4), 463 477. Littell, J.S., Peterson, D.L., Riley, K.L., Liu, Y., Luce, C.H., 2016. A review of the relationships between drought and forest fire in the United States. Global Change Biol. 22 (7), 2353 2369. Liu, X., 2003. Differential expression of genes regulated in response to drought or salinity stress in sunflower. Crop Sci. 43, 678 687. Liu, C.-W., Cheng, S.-W., Yu, W.-S., Chen, S.-K., 2003. Water infiltration rate in cracked paddy soil. Geoderma 117, 169 181. Liu, F., Xing, S., Ma, H., Du, Z., Ma, B., 2013. Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl. Microbiol. Biotechnol. 97, 9155 9164. Liu, X., Zhu, X., Pan, Y., Li, S., Liu, Y., Ma, Y., 2016. Agricultural drought monitoring: progress, challenges, and prospects. J. Geogr. Sci. 26, 750 767. Liverman, D.M., 1990. Drought impacts in Mexico: climate, agriculture, technology, and land tenure in Sonora and Puebla. Ann. Assoc. Am. Geogr. 80, 49 72. Loggini, B., Scartazza, A., Brugnoli, E., Navari-Izzo, F., 1999. Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol. 119, 1091 1100. Lu, S., Zhang, X., Bao, H., Skitmore, M., 2016. Review of social water cycle research in a changing environment. Renew. Sustain. Energy Rev. 63, 132 140.

Plant Life under Changing Environment

100

4. Regulation of drought stress in plants

Maes, W.H., Achten, W.M.J., Reubens, B., Muys, B., 2011. Monitoring stomatal conductance of Jatropha curcas seedlings under different levels of water shortage with infrared thermography. Agric. For. Meteorol. 151, 554 564. Manickavelu, A., Nadarajan, N., Ganesh, S.K., Gnanamalar, R.P., Chandra Babu, R., 2006. Drought tolerance in rice: morphological and molecular genetic consideration. Plant Growth Regul. 50, 121 138. Marini, I., Moschini, R., Del Corso, A., Mura, U., 2000. Complete protection by α-crystalline of lens sorbitol dehydrogenase undergoing thermal stress. J. Biol. Chem. 275, 32559 32565. Marulanda, A., Barea, J.M., Azco´n, R., 2009. Stimulation of plant growth and drought tolerance by native microorganisms (AM Fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J. Plant Growth Regul. 28, 115 124. Masaki, Y., Hanasaki, N., Takahashi, K., Hijioka, Y., 2015. Propagation of biases in humidity in the estimation of global irrigation water. Earth Syst. Dyn. 6, 461 484. Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., Suzuki, A., 2010. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann. Bot. 105 (7), 1141 1157. Matysik, J., Alia, Bhalu, B., Mohanty, P., 2002. Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr. Sci. 82, 525 532. McCoy, E.L., Stehouwer, R.C., 1999. Water and nutrient retention properties of internally porous inorganic amendments in high sand content root zones. J. Turfgrass Manage. 2, 49 69. Medina, A., Azco´n, R., 2010. Effectiveness of the application of arbuscular mycorrhiza fungi and organic amendments to improve soil quality and plant performance under stress conditions. J. Soil Sci. Plant Nutr. 10 (3), 354 372. Miller, G.L., 2000. Physiological response of bermudagrass grown in soil amendments during drought stress. HortScience 35, 213 216. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., Mittler, R., 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ. 33, 453 467. Mittler, R., Zilinskas, B.A., 1994. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J. 5, 397 405. Møller, I.M., Jensen, P.E., Hansson, A., 2007. Oxidative modifications to cellular components in plants. Annu. Rev. Plant Biol. 58, 459 481. Moret-Ferna´ndez, D., Gonza´lez-Cebollada, C., Latorre, B., 2012. Microflowmeter-tension disc infiltrometer—part I: Measurement of the transient infiltration rate. J. Hydrol. 466 467, 151 158. Morrissey, J.P., Dow, J.M., Mark, G.L., O’Gara, F., 2004. Are microbes at the root of a solution to world food production? EMBO Rep 5 (10), 922 926. Morte, A., Lovisolo, C., Schubert, A., 2000. Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almeriense-Terfezia claveryi. Mycorrhiza 10, 115 119. Mosley, L.M., 2015. Drought impacts on the water quality of freshwater systems; review and integration. EarthScience Rev. 140, 203 214. Mote, P.W., 2006. Climate-driven variability and trends in mountain snowpack in western North America. J. Clim. 19, 6209 6220. Mozaffari, K., Asadi, A.A., 2006. Relationships among traits using correlation, principal components and path analysis in safflower mutants sown in irrigated and drought stress condition. Asian J. Plant Sci. 5 (6), 977 983. Ngumbi, E., Kloepper, J., 2016. Bacterial-mediated drought tolerance: current and future prospects. Appl. Soil Ecol. 105, 109 125. Nihal, K., Terzi, R., Tekeli, C ¸ ., S¸ enel, G., Battal, P., Kadlogˇlu, A., 2009. Changes in anatomical structure and levels of endogenous phytohormones during leaf rolling in Ctenanthe setosa under stress drought. Turk. J. Biol. 33, 115 122. Nogue´s, S., Baker, N.R., 2000. Effects of drought on photosynthesis in Mediterranean plants grown under enhanced UV-B radiation. J. Exp. Bot. 51, 1309 1317. Ok, C.H., Anderson, S.H., Ervin, E.H., 2003. Amendments and construction systems for improving the performance of sand-based putting greens. Agron. J. 95, 1583 1590. Ortiz, N., Armada, E., Duque, E., Rolda´n, A., Azco´n, R., 2015. Contribution of arbuscular mycorrhizal fungi and/ or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J. Plant Physiol. 174, 87 96.

Plant Life under Changing Environment

References

101

¨ zkan, U., Go¨kbulak, F., 2017. Effect of vegetation change from forest to herbaceous vegetation cover on soil O moisture and temperature regimes and soil water chemistry. Catena 149, 158 166. Pace, P.F., Cralle, H.T., El-halawany, S.H.M., Cothren, J.T., Senseman, S.A., 1999. Drought-induced changes in shoot and root growth of young cotton plants. Methods 187, 183 187. Pandey, P., Irulappan, V., Bagavathiannan, M.V., Senthil-Kumar, M., 2017. Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front. Plant Sci. 8, 537. Pascual, I., Antolı´n, M.C., Garcı´a, C., Polo, A., Sa´nchez-Dı´az, M., 2004. Plant availability of heavy metals in a soil amended with a high dose of sewage sludge under drought conditions. Biol. Fertil. Soils 40, 291 299. Peleg, Z., Reguera, M., Tumimbang, E., Walia, H., Blumwald, E., 2011. Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol. J. 9, 747 758. Pinheiro, C., Chaves, M.M., 2010. Photosynthesis and drought: can we make metabolic connections from available data? J. Exp. Bot. 62, 869 882. Pinheiro, C., Chaves, M.M., 2011. Photosynthesis and drought: can we make metabolic connections from available data? J. Exp. Bot. 62, 869 882. Prasad, P.V.V., Staggenborg, S.A., Ristic, Z., 2008. Impacts of drought and/or heat stress on physiological, developmental, growth, and yield processes of crop plants. Response of crops to limited water: Understanding and modeling water stress effects on plant growth processes. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, pp. 301 355. Priyanka, B., Sekhar, K., Reddy, V.D., Rao, K.V., 2010. Expression of pigeonpea hybrid-proline-rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance. Plant Biotechnol. J. 8 (1), 76 87. Pustovoitova, T.N., Drozdova, I.S., Zhdanova, N.E., Zholkevich, V.N., 2003. Leaf growth, photosynthetic rate, and phytohormone contents in Cucumis sativus plants under progressive soil drought. Russ. J. Plant Physiol. 50, 441 443. Raghavendra, A.S., Gonugunta, V.K., Christmann, A., Grill, E., 2010. ABA perception and signalling. Trends Plant Sci. 15, 395 401. Ramı´rez, J.M., Dı´az, Y., Bedoya, J.G., 2017. Property tax revenues and multidimensional poverty reduction in Colombia: a spatial approach. World Dev. 94, 406 421. Rasmussen, S., Barah, P., Suarez-Rodriguez, M.C., Bressendorff, S., Friis, P., Costantino, P., et al., 2013. Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol. 161, 1783 1794. Reddy, A.R., Chaitanya, K.V., Vivekanandan, M., 2004. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J. Plant Physiol. 161, 1189 1202. Ren, D., Xu, X., Hao, Y., Huang, G., 2016. Modeling and assessing field irrigation water use in a canal system of Hetao, upper Yellow River basin: application to maize, sunflower and watermelon. J. Hydrol. 532, 122 139. Rezaei, M.A., Jokar, I., Ghorbanli, M., Kaviani, B., Kharabian-masouleh, A., 2012. Morpho-physiological improving effects of exogenous glycine betaine on tomato (Lycopersicum esculentum Mill.) cv. PS under drought stress conditions. Plant Omics J. 5, 79 86. Rhee, J.Y., Chung, G.C., Katsuhara, M., Ahn, S.J., 2011. Effect of nutrient deficiencies on the water transport properties in figleaf gourd plants. Hortic. Environ. Biotechnol. 52, 629 634. Rinalducci, S., Murgiano, L., Zolla, L., 2008. Redox proteomics: basic principles and future perspectives for the detection of protein oxidation in plants. J. Exp. Bot. 59, 3781 3801. Ristic, Z., Jenks, M.A., 2002. Leaf cuticle and water loss in maize lines differing in dehydration avoidance. J. Plant Physiol. 159, 645 651. Rizhsky, L., 2004. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134, 1683 1696. Rolda´n, A., Dı´az-Vivancos, P., Herna´ndez, J.A., Carrasco, L., Caravaca, F., 2008. Superoxide dismutase and total peroxidase activities in relation to drought recovery performance of mycorrhizal shrub seedlings grown in an amended semiarid soil. J. Plant Physiol. 165 (7), 715 722. Salami, H., Shahnooshi, N., Thomson, K.J., 2009. The economic impacts of drought on the economy of Iran: an integration of linear programming and macroeconometric modelling approaches. Ecol. Econ. 68, 1032 1039.

Plant Life under Changing Environment

102

4. Regulation of drought stress in plants

Saleem, M., Arshad, M., Hussain, S., Bhatti, A.S., 2007. Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol 34, 635 648. Salehi-Lisar, S.Y., Bakhshayeshan-Agdam, H., 2016. Drought stress in plants: causes, consequences, and tolerance. In: Drought Stress Tolerance in Plants, vol. 1. Springer, Cham, pp. 1 16. Saleska, S.R., Didan, K., Huete, A.R., Da Rocha, H.R., 2007. Amazon forests green-up during 2005 drought. Science (80) 318, 612. Salzmann, N., Huggel, C., Rohrer, M., Stoffel, M., 2014. Data and knowledge gaps in glacier, snow and related runoff research a climate change adaptation perspective. J. Hydrol. 518, 225 234. Sandhya, V., Ali, S.Z., Grover, M., Reddy, G., Venkateswarlu, B., 2010. Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul. 62, 21 30. Sato, Y., Yokoya, S., 2007. Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7. Plant Cell Rep. 27, 329 334. Schachtman, D.P., Goodger, J.Q.D., 2008. Chemical root to shoot signaling under drought. Trends Plant Sci. 13, 281 287. Schymanski, S.J., Or, D., 2015. Wind increases leaf water use efficiency. Plant. Cell Environ 39, 1448 1459. Scoffoni, C., Vuong, C., Diep, S., Cochard, H., Sack, L., 2014. Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance. Plant Physiol. 164, 1772 1788. Seabrook, L., McAlpine, C., Baxter, G., Rhodes, J., Bradley, A., Lunney, D., 2011. Drought-driven change in wildlife distribution and numbers: a case study of koalas in south west Queensland. Wildl. Res. 38, 509 524. Seghatoleslami, M.J., Kafi, M., Majidi, E., 2008. Effect of drought stress at different growth stages on yield and water use efficiency of five proso millet (Panicum Miliaceum L.) genotypes. Pak. J. Bot. 40, 1427 1432. Serraj, R., Sinclair, T.R., 2002. Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ. 25, 333 341. Shahattary, F.S., Mansourifar, C., 2017. The effect of drought stress on morphological and physiological traits and essence percentage of medicinal plant, Nigella sativa. Biosci. Biotechnol. Res. Commun. 1, 298 305. Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y., et al., 2002. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53, 1305 1319. Shinozaki, K., Yamaguchi-Shinozaki, K., 2007. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58, 221 227. Shinozaki, K., Yamaguchi-Shinozaki, K., Seki, M., 2003. Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant Biol. 6, 410 417. Silva, E.C. da, Nogueira, R.J.M.C., Silva, M.A. da, Albuquerque, M., 2011. Drought stress and plant nutrition. Plant Stress 5, 32 41. Smertenko, A., 2017. Can peroxisomes inform cellular response to drought? Trends Plant Sci. 22, 1005 1007. Spera, S.A., Galford, G.L., Coe, M.T., Macedo, M.N., Mustard, J.F., 2016. Land-use change affects water recycling in Brazil’s last agricultural frontier. Global Change Biol. 22, 3405 3413. Sperlich, D., Chang, C.T., Pen˜uelas, J., Gracia, C., Sabate´, S., 2015. Seasonal variability of foliar photosynthetic and morphological traits and drought impacts in a Mediterranean mixed forest. Tree Physiol. 35, 501 520. Stigter, E.M., Wanders, N., Saloranta, T.M., Shea, J.M., Bierkens, M.F.P., Immerzeel, W.W., 2017. Assimilation of snow cover and snow depth into a snow model to estimate snow water equivalent and snowmelt runoff in a Himalayan catchment. Cryosphere 11, 1647 1664. Subramanian, K.S., Charest, C., 1999. Acquisition of N by external hyphae of an arbuscular mycorrhizal fungus and its impact on physiological responses in maize under drought-stressed and well-watered conditions. Mycorrhiza 9, 69 75. Subramanian, K.S., Charest, C., Dwyer, L.M., Hamilton, R.I., 1995. Arbuscular mycorrhizas and water relations in maize under drought stress at tasselling. New Phytol. 129, 643 650. Subramanian, K.S., Santhanakrishnan, P., Balasubramanian, P., 2006. Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci. Hortic. (Amsterdam). 107, 245 253. Sun, W., Bernard, C., Van De Cotte, B., Van Montagu, M., Verbruggen, N., 2001. At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J. 27, 407 415.

Plant Life under Changing Environment

References

103

Sunderland, T., Apgaua, D., Baldauf, C., Blackie, R., Colfer, C., Cunningham, A.B., et al., 2015. Global dry forests: a prologue. Int. For. Rev. 17, 1 9. Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., et al., 2002. Important roles of droughtand cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29, 417 426. Terzi, R., Saruhan Gu¨ler, N., Kutlu C ¸ ali¸skan, N., Kadiogˇlu, A., 2013. Lignification response for rolled leaves of Ctenanthe setosa under long-term drought stress. Turkish J. Biol. 37, 614 619. Thomas, J., Prasannakumar, V., 2016. Temporal analysis of rainfall (1871 2012) and drought characteristics over a tropical monsoon-dominated State (Kerala) of India. J. Hydrol. 534, 266 280. Todaka, D., Shinozaki, K., Yamaguchi-Shinozaki, K., 2015. Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front. Plant Sci. 6, 84. Toumi, I., Gargouri, M., Nouairi, I., Moschou, P.N., Ben Salem-Fnayou, A., Mliki, A., et al., 2008. Water stress induced changes in the leaf lipid composition of four grapevine genotypes with different drought tolerance. Biol. Plant. 52, 161 164. Umezawa, T., Fujita, M., Fujita, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., 2006. Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr. Opin. Biotechnol. 17, 113 122. van Dijk, A.I.J.M., Beck, H.E., Crosbie, R.S., de Jeu, R.A.M., Liu, Y.Y., Podger, G.M., et al., 2013. The Millennium Drought in southeast Australia (2001 2009): natural and human causes and implications for water resources, ecosystems, economy, and society. Water Resour. Res. 49, 1040 1057. Vardharajula, S., Zulfikar Ali, S., Grover, M., Reddy, G., Bandi, V., 2011. Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J. Plant Interact. 6, 1 14. Vicente-Serrano, S.M., Gouveia, C., Camarero, J.J., Begueria, S., Trigo, R., Lopez-Moreno, J.I., et al., 2013. Response of vegetation to drought time-scales across global land biomes. Proc. Natl. Acad. Sci. U.S.A. 110, 52 57. Vurukonda, S.S.K.P., Vardharajula, S., Shrivastava, M., SkZ, A., 2016. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol. Res. 184, 13 24. Walter, J., Hein, R., Auge, H., Beierkuhnlein, C., Lo¨ffler, S., Reifenrath, K., et al., 2012. How do extreme drought and plant community composition affect host plant metabolites and herbivore performance? Arthropod. Plant. Interact. 6, 15 25. Wan, W., Zhao, J., Li, H.Y., Mishra, A., Ruby Leung, L., Hejazi, M., et al., 2017. Hydrological drought in the anthropocene: impacts of local water extraction and reservoir regulation in the U.S. J. Geophys. Res. Atmos. 122, 11313 11328. Wanders, N., Wada, Y., 2015. Human and climate impacts on the 21st century hydrological drought. J. Hydrol. 526, 208 220. Wang, W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1 14. Wang, M., Zheng, Q., Shen, Q., Guo, S., 2013. The critical role of potassium in plant stress response. Int. J. Mol. Sci. 14, 7370 7390. Wehner, G.G., Balko, C.C., Enders, M.M., Humbeck, K.K., Ordon, F.F., 2015. Identification of genomic regions involved in tolerance to drought stress and drought stress induced leaf senescence in juvenile barley. BMC Plant Biol. 15, 125. Wehtje, G.R., Shaw, J.N., Walker, R.H., Williams, W., 2003. Bermudagrass growth in soil supplemented with inorganic amendments. HortScience 38, 613 617. Wilhite, D.A., 2002. Combating drought through preparedness. Nat. Resour. Forum 26, 275 285. Wilkinson, S., Davies, W.J., 2010. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ. 33, 510 525. Wilkinson, S., Kudoyarova, G.R., Veselov, D.S., Arkhipova, T.N., Davies, W.J., 2012. Plant hormone interactions: innovative targets for crop breeding and management. J. Exp. Bot. 63, 3499 3509. Wittenmayer, L., Merbach, W., 2005. Plant responses to drought and phosphorus deficiency: contribution of phytohormones in root-related processes. J. Plant Nutr. Soil Sci. 168, 531 540. Wu, P., Tan, M., 2012. Challenges for sustainable urbanization: a case study of water shortage and water environment changes in Shandong, China. Procedia Environ. Sci. 13, 919 927.

Plant Life under Changing Environment

104

4. Regulation of drought stress in plants

Xiang, D.B., Peng, L.X., Zhao, J.L., Zou, L., Zhao, G., Song, C., 2013. Effect of drought stress on yield, chlorophyll contents and photosynthesis in tartary buckwheat (Fagopyrum tataricum). J. Food Agric. Environ. 11, 1358 1363. Xoconostle-Ca´zares, B., Ramı´rez-Ortega, F.A., Flores-Elenes, L., Ruiz-Medrano, R., 2010. Drought tolerance in crop plants. Am. J. Plant Physiol. 5, 241 256. Xu, Z., Zhou, G., Shimizu, H., 2010. Plant responses to drought and rewatering. Plant Signal. Behav. 5, 649 654. Yamaguchi, A., Hiyoshi, N., Sato, O., Shirai, M., 2011. Sorbitol dehydration in high temperature liquid water. Green Chem. 13, 873. Yang, F., Miao, L.F., 2010. Adaptive responses to progressive drought stress in two poplar species originating from different altitudes. Silva Fennica 44 (1), 23 37. Yang, J., Kloepper, J.W., Ryu, C.M., 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14, 1 4. Yang, H., Zhao, L., Zhao, S., Wang, J., Shi, H., 2017a. Biochemical and transcriptomic analyses of drought stress responses of LY1306 tobacco strain. Sci. Rep. 7, 17442. Yang, W., Tan, R.T., Feng, J., Liu, J., Guo, Z., Yan, S., 2017b. Joint rain detection and removal via iterative region dependent multi-task learning. CVPR 2, 1 12. You, J., Hu, H., Xiong, L., 2012. An ornithine δ-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Sci. 197, 59 69. Yousfi, N., Slama, I., Ghnaya, T., Savoure´, A., Abdelly, C., 2010. Effects of water deficit stress on growth, water relations and osmolyte accumulation in Medicago truncatula and M. laciniata populations. Comptes Rendus Biol. 333, 205 213. Zandalinas, S.I., Mittler, R., Balfago´n, D., Arbona, V., Go´mez-Cadenas, A., 2018. Plant adaptations to the combination of drought and high temperatures. Physiol. Plant. 162, 2 12. Zargar, S.M., Gupta, N., Nazir, M., Mahajan, R., Malik, F.A., Sofi, N.R., et al., 2017. Impact of drought on photosynthesis: molecular perspective. Plant Gene 11, 154 159. Zeppel, M.J.B., Harrison, S.P., Adams, H.D., Kelley, D.I., Li, G., Tissue, D.T., et al., 2015. Drought and resprouting plants. New Phytol. 206, 583 589. Zhang, J., Jia, W., Yang, J., Ismail, A.M., 2006. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res. 97, 111 119. Zhou, J., Wang, X., Jiao, Y., Qin, Y., Liu, X., He, K., et al., 2007. Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol. Biol. 63, 591 608. Zhu, J.-K., 2016. Abiotic stress signaling and responses in plants. Cell 167, 313 324. Zhu, T., Budworth, P., Han, B., Brown, D., Chang, H.-S., Zou, G., et al., 2001. Toward elucidating the global gene expression patterns of developing Arabidopsis: parallel analysis of 8300 genes by a high-density oligonucleotide probe array. Plant Physiol. Biochem. 39, 221 242. Zhu, X.G., Wang, Y., Ort, D.R., Long, S.P., 2013. e-Photosynthesis: a comprehensive dynamic mechanistic model of C3 photosynthesis: from light capture to sucrose synthesis. Plant, Cell Environ. 36, 1711 1727. Zickfeld, K., Solomon, S., Gilford, D.M., 2017. Centuries of thermal sea-level rise due to anthropogenic emissions of short-lived greenhouse gases. Proc. Natl. Acad. Sci. U.S.A. 114, 657 662. Zlotorowicz, A., Strand, R.V., Burheim, O.S., Wilhelmsen, Ø., Kjelstrup, S., 2017. The permselectivity and water transference number of ion exchange membranes in reverse electrodialysis. J. Memb. Sci. 523, 402 408. Zulini, L., Rubinigg, M., Zorer, R., Bertamini, M., 2007. Effects of drought stress on chlorophyll fluorescence and photosynthetic pigments in grapevine leaves (Vitis vinifera cv. ‘White Riesling’). In: Acta Horticulturae. pp. 289 294.

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5 Plant responses to radiation stress and its adaptive mechanisms Shikha Singh, Abreeq Fatima, Santwana Tiwari and Sheo Mohan Prasad Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India

5.1 Introduction During the past few decades, obliteration of forests and scorching of fossil fuels have led to the accumulation of greenhouse gases, such as carbon dioxide, methane, chlorofluorocarbons, nitrous oxide, and tropospheric ozone, which permit solar radiation to reach the earth surface (Worrest et al., 1989; Dawson, 1992). This outgoing radiation is absorbed and reradiated by greenhouse gases, effectively storing some amount of the heat in the atmosphere and producing a net heat to the earth surface. After that, the quantity of greenhouse gases is still increasing and causes climatic change, which is predicted to produce global warming. Climate change studies are of considerable importance in agricultural and environmental science. Responses of the plant to various environmental stresses are governed by complex molecular and biochemical signal transduction processes, acting in coordination to determine tolerance or sensitivity at the whole plant level. Radiation stresses, including ultraviolet (UV)-B (UV-B) irradiance, trigger a wide array of plant responses, ranging from altered gene expression and cellular metabolism (e.g., membrane injuries, photosynthetic disorders) to changes in growth rates and crop yields (Fig. 5.1). Upon exposure to biotic and abiotic stresses, plants express a sophisticated and coordinated response to reprogram interconnected defense networks and numerous physiological, molecular, and cellular adaptations. Solar radiation is an important part of sustainable life on earth. Since the agricultural system round the globe is facing trouble in coping up with the massive population, its feeding needs and this hunger list are expected to surpass 2.3 billion by 2050 (FAO, 2009), which will lead to poverty and consumption of scarce natural resources, whereas the productivity is not increasing in proportion to the population

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FIGURE 5.1 Schematic representation of overall mechanism adapted by plant under the stress condition of harmful radiation.

growth due to various underlying causes among which UV radiation (UVR) hits the list. Solar radiation is a set of electromagnetic radiations emitted by the sun, which ranges from infrared (IR) to UV (200 and 4000 nm), and reaches the earth surface through sunlight. Life promoted on earth by light energy derived from the sun, which is the major source for photoautotrophs, are mainly fixed in the presence of chlorophyll. Apart from being an energy source, light also acts as a major environmental indication for plants to synchronize and adjust with its surrounding condition. In nature, solar radiation comprises different wavelengths of electromagnetic waves and is broadly classified as UVR (UV , 400 nm), photosynthetically active radiation (PAR; B400 700 nm), and far red radiation (B700 780 nm). Not all the wavelengths are absorbed by the plant, only PAR is considered as the active region for autotrophs. The depletion of the stratospheric ozone layer is leading to an enhanced rate in UV-B (280 320 nm) radiation reaching the earth’s surface. This has raised interest in the possible consequence of increased UV-B levels on the growth and development of plant and the mechanisms underlying these responses. Although the effects of UV-B are now well characterized at the physiological level, very little is known about the cellular and molecular mechanisms involved therein. Some recent studies have shown that UV-B affects a number of important physiological processes, such as photosynthesis, through effects on gene expression (Fig. 5.1). In addition, induction of a number of defense related mechanisms, such as production of UV-B screening pigments, increase in antioxidant enzymes content, and induction of pathogenesis-related (PR) proteins are also mediated at the level of gene expression. Solar radiation conveys energy for the metabolic process of the plants. Mainly, photosynthetic assimilates are synthesized as vegetal components from water, CO2, and light energy. Apart from this, energy is also used in evaporation by different parts of the plants, and also in the transpiration through stomata. Under any abiotic stress, a major effect is noticed on the plant cell. The potential of the plant cell is in accordance with that of the environment surrounding the cell. One of

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the frequently reported responses to UV-B is a reduction in the rate of photosynthesis. The photosynthetic system, by its nature, is vulnerable to UV-B damage and a number of targets for UV-B damage within the chloroplast and photosynthetic apparatus have been identified (Bornman, 1989). However, recent studies have shown that under realistic UV-B conditions, reduction in RuBisCO levels is the primary cause for the decline in the rate of photosynthesis (Allen et al., 1997; Baker et al., 1997). This chapter describes the recent developments in our understanding of the mechanisms, specifically its effects on morphophysiological, biochemical, and molecular changes in plants responses to radiation stress (Fig. 5.1).

5.2 Plants and their environment 5.2.1 Source of life on earth In its various forms, sunlight is a strength that has built up and driven the amazing living matters of this planet for a long time billions years ago. ‘It represents the finest engineering as well as broadest safety margin hence, the greatest design we experience today. It provides amply for our needs, yet limits our greed. It is safe, eternal, universal and frees’ (Theodore B. Taylor, 1977).

Plants, the base components of any ecosystem, are completely reliant on solar energy and sunlight is the ultimate source which drives photosynthesis and directs the progress of the plants from seedling stage to the emergence of tiny coleoptiles up to the blooming. Since the life on earth is sustained by the green plants and cyanobacteria for our survival, beginning from O2 to carbohydrate, we are totally dependent on the primary producers of terrestrial and aquatic ecosystem. However, sunlight is not always beneficiary, but it can also exert catastrophic effects. Therefore proper measurement is crucial for a plant to utilize the solar radiation efficiently without suffering the damage. To drive photosynthetic processes, plants require sunlight and, therefore, are exposed to the UVR which falls into three categories: UV-A, UV-B, and UV-C. On the evolutionary front, plants have gained the ability to sense the quality, intensity, direction, and duration of light with an exception to sense UV-B besides blue and red lights. Various studies suggest the induction of growth responses by UV-B causing morphological and physiological changes in plants including DNA damage. Well surprisingly it is not only a bad news that UVR also plays an important evolutionary role in promoting mutations which leads to new traits, and drives the development of species diversity. However, mutations impact negatively most of the time resulting into cellular dysfunction even leading to cell death. Fascinatingly, plants also exploit blue and UV wavelengths to direct DNA repair processes.

5.2.2 Types and sources of radiation The atmosphere acts as a blanket and as a filter too which filters out the bands of wide range of astral bands at its diverse sheets as cosmic rays pass through it to the earth’s surface, to facilitate only a fraction of it reaches the surface. The atmosphere absorbs only some parts of the radiation, some sent to the earth, and the rest directed back to space,

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which then is irradiated. A thermal balance yielded by all of these radiations result in radiant symmetry. Solar radiation can be classified broadly under two categories. (1) Radiation which directly comes from the sun without any change in its direction is referred to as “direct radiation.” This radiation is characterized by projecting a defined shadow onto the objects that intersect it. (2) This type of radiation is mainly derived as a result of reflection and scattering by clouds, dust particles, mountains, trees, buildings, and the ground itself, so on and so forth, that is, from all over the atmosphere, which is called “diffuse radiation.” The amount of direct radiation is greater than diffused radiation in a clear sky on a vibrant sunny day. Radiation is a dynamic power that travels through space and is able to penetrate various objects and materials. To acquire the stability the atoms with unstable nuclei emit the excess of energy termed as emission which is categorized into the following: (1) Nonionizing radiation—this radiation has relatively low energy. Nonionizing radiation refers to the portion of the electromagnetic spectrum together with UV spectrum, visible light, IR, microwave, radio frequency, and extremely low frequency. The penetration ability of these radiations over tissue is dependent on the particular wavelength, which will determine the site and category of biological consequences. Most of the evidences point out that the nonionizing radiation has no serious ill effects, although some studies have found possible effects. (2) Ionizing radiation—ionizing radiation produces charged particles or ions on hitting any object but they are incapable of breaking molecular bonds or removing electrons. This radiation energy is transferred by particles or waves containing a high amount of energy and these high-energy ionizing radiations can lead to serious problems within plants and cyanobacteria. Ionizing radiation may yield few other forms of radiations instigated by unstable atoms having either excessive energy or mass (or both), namely, alpha, beta, gamma, neutron particles, and X-rays. 5.2.2.1 Alpha radiation It occurs when an atom undergoes radioactive decay, and releases a particle called alpha particle having two protons and two neutrons. Although these particles are incapable of penetrating the outer layer of dead skin cells, but if they are ingested in food or air, they cause serious cell damage. 5.2.2.2 Beta radiation Beta radiation takes the form of either an electron or being emitted from an atom. Since a beta particle is very small in size and light in weight, it is able to travel further in air, up to a few meters, and is able to puncture the skin up to a few centimeters, posing an external health risk. However, the main threat is inflicted by internal emission through ingested material. It is reported that submerged roots of Lemna minor plants were more radiosensitive to β-radiation as compared to the floating fronds and poses a negative impact. 5.2.2.3 Gamma radiation Gamma rays have a huge amount of energy around 10 to hundreds of keV and are considered to be the most deeply penetrating among others (Kovacs and Keresztes, 2002). It does not consist of any particles; instead, it consists of a photon of energy being emitted from an unstable nucleus having no mass or charge. Hence, it can travel much farther through air than alpha or beta. It has also been reported by several scientists that gamma

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waves can be stopped by a thick layer of material, with high atomic number such as lead or depleted uranium, which are quite effective in shielding. It is reported by Salter and Hewitt (1992) that gamma irradiation causes overproduction of reactive oxygen species (ROS) which rapidly reacts with almost other structural and functional organic molecules and disturbs homeostasis. It is revealed that increased dosage of gamma radiation can cause reduction in chlorophyll a and b concentrations and it is proved that the plantlets irradiated with gamma radiation have a lower amount of chlorophyll a and b with respect to the nonradiated one. 5.2.2.4 X-rays X-ray radiations are quite similar to gamma radiation, with the only difference that they emerge from the electron cloud due to energy changes in an electron, such as moving from a higher energy level to the lower one, releasing excess amount of energy. These radiations have longer wavelength and lower energy than gamma radiation. 5.2.2.5 Ultraviolet radiation UVR is a type of electromagnetic radiation whose wavelength ranges between 100 and 400 nm, highly energetic radiation representing about 7% 9% of the total solar radiation in the biosphere. Almost all the UV-C (,280 nm), a significant part of UV-B (280 315 nm) is absorbed by the stratosphere, but most of the UV-A radiation (315 400 nm) is transmitted to the surface of earth. It means that UVR can cause reactions between molecules hitting them. Most of the UV solar radiation is absorbed by the stratospheric ozone layer and therefore UV-B (280 315 nm) is only a minor component of solar radiation at the earth’s surface. Among UVR types, UV-A radiation has been shown to have less DNA damaging effect because it cannot be absorbed by native DNA, whereas UV-A and visible light energy (up to 670 700 nm) can damage DNA via indirect photo-sensitizing, reaction-mediated ROS generation, especially singlet oxygen (1O2). At the end of UV spectrum, the colors of the rainbow start appearing. The amount of solar radiation outside the earth’s surface is more or less constant. The amount of the radiation harmful to the plant or organisms is determined by how much radiation an organism receives, as well as how long it is exposed to it. UV-B radiation is an important environmental signal, and has an extensive impact on the biosphere. In addition to its direct effects on organisms, UV-B impinges on numerous processes that affect metabolism, development, and viability that involves differential regulation of gene expression. The response of different organisms to UV-B not only depends on the nature of the treatment, the extent of adaptation and acclimation but also on the interaction with other environmental factors.

5.3 Effect of radiations Several scientists have focused their research regarding the damaging effects of UV-B radiation on various vital processes of different organisms including cyanobacteria and plants (Hader et al., 2007; Rastogi et al., 2011; Santos et al., 2012; Oliveira et al., 2016; Singh et al.,2019). The negative impact of UV-B radiation on most organisms is mediated by free

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radicals which induce oxidative stress. The overproduction and accumulation of reduced oxygen intermediates can affect proteins, DNA and lipids vigorously as demonstrated by Kumar et al. (2016) in their work. Radiation affects plants as well as microorganisms on several aspects: morphologically, physiologically, and molecularly as well as biochemically. Although every parameter is a lifeline for them, damage or regression in any one of them disturbs their life processes. Sensitivity toward light exposes a very colorful world to human beings but the color of the world for some other organisms is not like it seems to us. For example, the vision of bees, butterflies, and other insects extends into the UV range of spectrum and hence, many insects can visualize the accumulation of UV-absorbing pigments by plants. Thus on the evolutionary scale a mutual plant pollinator relationship is developed by the color vision of some insects and the spectral properties of flowers. Plants are an essential resource for humans in different ways for different purposes. Basically, photosynthesis is the process in which each atom of carbon and minerals coming from the soil which builds our body is first taken up by plants and fixed chemically, after which it can be exploited by us; the same is true for minerals also. Apart from this, plants also produce many important protective substances and vitamins that contribute to our benefits as our bodies are not able to synthesize those. Phenolics are also powerful antioxidants, can chelate with divalent metal ions such as iron and copper, and allow our body to use these micronutrients. Some major sources of phenolics include medical plants, grains, fruits and vegetables, tea coffee, bee pollen, and red wine. The synthesis of different phenolic compounds (i.e., flavonoids, stilbenes) and vitamin D production is stimulated by UV-B. Stimulation of UVR has also been known to enhance the production of different alkaloids, phenolics, and essential oils. Extensive studies on UVR explain that UV-B radiation increases the amount of active substances in many plant species.

5.3.1 Morphological and physiological effects Numerous studies have examined the effects of UV-B on plants; it influences various developmental processes and modifies plant architecture. With the ability to exploit sunlight, plants also have some means of protecting the living cells from the damages of cell membranes and DNA (Stefi et al., 2016). Sensitivity to UV-B includes stunted growth and leaf area, glazing and burning of leaf. There is a drastic decrease in overall biomass production. Portioning of growth to different organs like altered leaf area and internode of the plants; such effects appear differently in different plants (Teramura, 1983). Seedlings are highly susceptible to UVR as are mature plants undergoing transition from vegetative to reproductive phase (Teramura, 1987). A wide range of responses at the cellular level along with biosynthesis of protein, nitrogen fixation, photosynthesis has been observed by the treatment with UV-B radiation, as it was reported in many studies concerning cyanobacteria (Kumar et al., 2003; Dillon et al., 2003). The phycobilin proteins behaving as solar energy harvesting antennae are specifically bleached by UVR, though various reports have demonstrated an adaptation to UV stress and an increased resistance could also be devised. Cyanobacteria increases their resistance to UV-B by adaptive mutagenesis as reported by many researchers (Sinha et al., 2005; Jiang and Qiu, 2005; Rajagopal et al., 2005; Helbling et al., 2006). Furthermore, responses to UV-B modify plant biochemical

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composition, influence plant morphology, and help to deter pests and pathogens. Since photosynthesis is an essential process for survival of every autotroph, PAR is required. PAR shows large seasonal and diurnal changes, and its intensity is also influenced by meteorological factors. When the photon intensity is within the range of utilizing capacity of chloroplasts for CO2 fixation, photosynthesis runs efficiently without any hindrance caused by biochemical factors (Hideg et al., 2002), but it is well reported in several studies that net photosynthesis is severely inhibited by several factors including UV-B radiation. This hindrance could be due to increase in ROS generation than its scavenging mechanism. Similar deterioration in the photosynthesis rate was also observed in green alga by White and Jahnke (2002) by exposure of UV rays. Effects of the electromagnetic field were also considered as damaging for photosynthetic cells of tobacco by causing damage in the membrane of photosynthetic cells in leaves by decreasing photochemical efficiency of photosystems. Deactivation of photosystem II (PS II) may also be the consequence of degradation of several pigments which governs the process. As stated by Fukuchi et al. (2004), UV-A has the ability to decompose the UV-B absorbing pigment, thereby reducing the capacity of the plants to fight off UV-B stress. Inhibition of epidermal cell elongation is by UV-6 and UV-C is another UVR response reported in sunflower seedlings. The other well-studied response to UV-B radiation is damage to the photosynthetic apparatus and among different photosynthetic components, PS II is UV-B sensitive but the action spectrum of the UV-6 effect does not suggest a specific target molecule. The damage in the photosynthetic apparatus is measured by a rise in variable chlorophyll fluorescence (Tevini et al., 1991) radiation. In the context of pollen development and germination processes, Chauhan and Katiyar (1998) found the inhibition in both the processes by increasing the intensity of gamma rays. After enhanced UV-B exposure, reduced performance of pollen gains has also been reported by Koti et al. (2005) in soybean where various agrobiochemical changes in reproductive organs have been linked to UV-B radiation. Furthermore, it has also been known since an earlier period that gamma rays have both positive and negative impacts on the growth and development process of plants (McCormick and Platt, 1962). Akbal et al. (2012) have documented that plant seeds are being affected even in dormancy state while the growth of plants was significantly inhibited when irradiated with a high dose gamma radiation as reported by Wi et al. (2007). Stefi et al. (2016) also demonstrated an experiment with Arabidopsis thaliana plant under nonionizing radiation to carry out structural and biochemical alternation. They showed that plants have thinner leaves and possess fewer chloroplasts compared to their control counterparts when exposed to nonionizing radiation emitted from the base unit of a cordless digital enhanced cordless telecommunications (DECT) system.

5.3.2 Biochemical changes As stated by Hideg et al. (2002), all the photoautotrophs including plants and cyanobacteria depend on light for their basic life processes, that is, photosynthesis, biosynthesis of cell components, photo-morphogenesis, and development. In terms of intensities of solar radiation and its spectral distribution in plant species and their developmental stages, the light requirements are largely flexible. ROS at high concentration are extremely harmful to living organisms. They are generated by stepwise reduction of molecular oxygen (O2) and by the electron-transfer reactions leading to production of the highly reactive ROS.

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Generation of ROS depends on the utilizing capacity of chloroplast for CO2 fixation. It is very low when the intensity of photon is within the range and can be very efficiently scavenged. When either PAR intensity is high or quenching capacity of chloroplast is low due to any stressor, the scavenging capacity gets affected negatively and ROS starts accumulating and causing hindrance in the photosynthesis process. In general, stress responses and possibly necrosis was observed upon exposure of high fluence rates with short wavelengths of UV-B, whereas low fluence rates with longer wavelengths induce a variety of genes, a number of which are known to be involved in UV protection or the amelioration of UV damage. Several other reports have been documented related to the damaging effect of UV-B to DNA, proteins, and membrane lipids, and also the inhibition of protein synthesis (Nawkar et al., 2013; Stefi et al., 2016; Bashri et al., 2017). Yadav et al. (2016) reported that UV-B might cause the ROS production by disturbing the normal reduction pathway of NADP1 to NADPH during photosynthetic electron transport chain. The generation of ROS might be due to oxidation of lipid and proteins. One of its consequences is excessive generation or accumulation of malondialdehyde content which is the cause of severe disturbances in the membrane integrity that may lead to senescence and ultimately, death. Lipid peroxidation and free radical generation are majorly considered as agents for leaf senescence. When the level of ROS increases, it damages the chlorophyll leading to chlorosis. With references to gamma rays it causes damaging effects to the biomolecules by conformational changes, rupturing the covalent bonds, and through production of free radicals. This may happen because of excessive generation or acquisition of ROS or when the defense mechanism is checked out which leads to the destruction of functional protein, inactivation of enzymes, oxidation of lipids, and changing confirmation of nucleic acids. Halliwell and Gutteridge (1986) justified that the oxidative radicals such as hydroxyl ion and superoxide anion could modify the specific molecular properties of the cell. Varying exposures of eukaryotic cells to ionizing radiation may result in the immediate formation of free radicals lasting only for a matter of milliseconds and cause oxidative stress through radiolysis of body water contents, which is often referred to as the indirect effect of radiation. When it is coupled with oxygen effect (detrimental effect of ionizing radiation due to the presence of oxygen), the chances of tissue injury enhance manifold. Consequently, low or high doses of ionizing radiation were used to stimulate or inhibit seed germination, plant growth and development in various plant and animal organisms (Sagan, 1987; Korystov and Narimanov, 1997; Sreedhar et al., 2013). In addition to this, UV-B was reported to modify the metabolism and promote synthesis of a range of secondary metabolites, including the UV-protective flavonoids (Mewis et al., 2012).

5.3.3 Molecular damages The effect of high levels of different radiations on organisms includes chromosomal aberration, which is responsible for changes in the structure of chromosome. Inversions and deletions are the commonest type of DNA damage resulting in altered DNA sequences. This affects via massive reduction in the growth rate, which is speculated as a reduction in the rate of growth of organisms. It is reported that reproduction is negatively correlated with UV stress encompassing sterility, occurrence of developmental abnormalities, or reduction in viability of offspring. In various plant species, UV-B radiation can

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change the ultrastructure of cellular components which is generally caused by damage and dilation of the nuclear membrane. It is evident that UV rays are dangerous for plants as it directly alters the rate of seed germination, rate of mortality, including enhancements to both acute lethality and long-term reduction in the life span of plants and cyanobacteria. In the early Precambrian era, fluxes of solar radiation including UV-B and UV-C at the surface of the earth were several-fold higher than today due to the lack of oxygen in the atmosphere. Recent reports suggest that UV-B radiation treatment results in a wide range of responses at the cellular level. While on the other hand at the molecular front, varied range of responses appear upon UV exposure. The stress signal is subsequently amplified and transmitted using cyclic nucleotides as secondary messengers followed by the production of shock proteins. UV-B has the highest energy of any part of the daylight radiation bands and has the capacity to damage macromolecules as well as to generate ROS and impair cellular processes. In addition to prolonged UV-B exposures an adaptation to the ROS stress has been documented. DNA absorbs UVR in three spectral regions: (1) with a peak at 260 264 nm, (2) with a peak at 192 nm, and (3) below 125 nm. Chloroflexus aurantiacus, a primarily photoheterotrophic anoxygenic bacteria, showed relatively high UV-C tolerance which may have had relevance during the Archean era when the Chloroflexi may have evolved (Pierson et al., 1993). DNA is one of the most significant targets of UVRs. It is well reported that elevated level of UV-B can damage DNA and proteins (Bashri et al., 2017) resulting in the inactivation of PS II by downregulating the genes of RuBisCO enzymes, namely, rbcS and rbcL and also the genes of light harvesting complex, namely, Lhcb and psbA (Zlatev et al., 2012). As DNA is considered as the basic life unit, it gets easily damaged by UV-B radiation because it causes phototransformations that results in the production of cyclobutane pyrimidine dimers (CPDs) and pyrimidine, pyrimidinone dimers (Hader et al., 2007). DNA damage resulted in (1) disincorporation of bases during replication process causing hydrolytic damage, (2) which results in deamination of bases continuation with depurination and depyrimidination, (3) oxidative damage, caused by direct interaction of ionizing radiation with DNA molecule. Basically, DNA protein cross-links with one another, the DNA strand breaks and deletion or insertion of base pairs can also be induced by UVRs. The process of leaf senescence is thought to be under genetic control and UV-B exposure controlled the induction of a number of genes associated with senescence such as senescence-associated genes (SAG) 12, 13, 14, and 17. In addition, John et al. (2001) while conducting his experiment with A. thaliana under UV-B exposure reported chlorophyll defeat and increased lipid damage in a parallel way to natural senescence. A number of these senescence-associated genes have been cloned and sequenced which may be involved in protein degradation and nitrogen remobilization. Genes encoding proteases (SAG 12), glutamine synthase (Atgsr2), ACC synthase (ACS6), lipases, glyoxylate cycle enzymes, and polyubiquitin are some of the identified clones of senescence-associated genes.

5.4 Mitigating strategies To combat the harmful UV rays, plants have developed different defense mechanisms. Deposition of UV-absorbing phenolic compounds in epidermal tissues in higher plants is

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one of the most important protective mechanisms. These phenolic compounds act as a sunblock, reducing penetration of rays into the leaf. Flavonoids and soluble hydroxyl cinnamic acid derivate appear to be the most important, as was shown for many plant species, including cereals. Effects of exposure to different radiations on various physiological processes in plants and mitigation strategies are represented in Table 5.1. Flavonoid accumulation in epidermal cells was shown to reduce transmittance, hence providing protection against UVR as reported by Tevini et al. (1991). Further, they reported in their study that the thicker and smaller leaves produced more flavonoids and anthocyanins. The mitigation strategies against radiation hassle could be categorized in the following subheadings.

5.4.1 Endogenous strategies Photoreactivation and photolyases have been extensively reported in several plant species (Yamamoto et al., 2007). However, credible work has been performed by many authors (Kumagai and Sato, 1992; Hidema et al., 2005; Teranishi et al., 2012) on Oryza sativa cultivars, where an enzyme photolyase has been proven as a major factor that modulate the DNA damage repairing capability of O. sativa cultivar. Furthermore, in case of cyanobacteria the protective and mitigating strategies include mat or crust formation, vertical migration of individuals within the mat. The surface layer of microbial mats often serves as a protector for the organisms underneath. A mat in a high Arctic lake showed high concentrations of photosynthetic pigments in the lower part of the mat, while the black top layer was rich in scytonemins and MAAs.

5.4.2 Ultraviolet shielding and behavioral escape mechanisms Synthesis of UV-absorbing compound is an important mechanism to prevent the UV photo-damage. Some of these adaptive strategies evolved in cyanobacteria probably did so in the Archean and early Proterozoic era, and may now represent relics of that time. Several studies provide evidence that MAAs protect cyanobacteria and other lower organisms by absorbing harmful UVR (Scherer et al., 1988; Karentz et al., 1991; Ehling-Schulz et al., 1997). By producing UV-absorbing substances including MAAs and/or scytonemins, many cyanobacteria are able to withstand excessive solar UVR (Liu et al., 2004). MAAs are water-soluble compounds and have absorption maxima in the range of 310 360 nm (Hidema et al., 2005). Upon absorption of UVR, MAAs form triplet states which thermally relax and thus render the radiation energy harmless (Conde et al., 2004). MAAs are either constitutive elements within the cells or are induced by solar radiation (Sinha and Hader, 2003). In many cases, action spectroscopy has shown that solar UV-B (which peaks around 300 nm) induces MAA synthesis in algae and phytoplankton, while visible radiation has no effect (Sinha et al., 2003). Scytonemins are yellowish-brown, lipid-soluble dimeric pigment with a molecular mass of 544 Da and structure based on indolic and phenolic subunits, exclusively synthesized by cyanobacteria, and are chemically very stable. Biosynthesis of scytonemin is induced by exposure to UV-A radiation and can be enhanced by elevated temperatures and photooxidative conditions. They can accumulate in sediments; their abundance in sediment cores has

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TABLE 5.1 The range of ultraviolet (UV) radiation and its effect on higher plants as well on lower organism. S. Radiation no types

Model system

Mitigation strategies Indole acetic acid, gibberellic acid, and kinetin

Effect

References

Lower dose stimulated pollen germination and tube growth, but higher dose was found to be inhibitory. Upon phytohormones application germination and tube elongation of pollen was promoted.

Chauhan and Katiyar (1998)

1.

γ-Radiation

Pinuskesiya Royal ex Gord

2.

UV-B

Poa pratensis Salicylic acid L.

Photochemical efficiency, antioxidants, such as α-tocopherol, SOD, CAT, and protective pigment, such as anthocyanin, were reduced under the influence of UV-B but it was alleviated by application of salicylic acid.

3.

UV-B

Solanum lycopersicum L.

Kinetin

Under the influence of UV-B the growth, Bashri et al. (2017) photosynthetic activities and values of chlorophyll a fluorescence parameters were reduced while energy flux parameters values and respiration rate were increased. Enzymes involved in nitrogen metabolism were also inhibited. Exogenously applied kinetin was found to ameliorate all the parameters.

4.

UV-B

Scutellaria baicalensis

Jasmonic acid

Under the influence of UV-B radiation photosynthesis inhibition and decreased biomass in stem and leaves were noticed. Recovery in photosynthesis was noticed in the presence of jasmonic acid by the recovery of chlorophyll content, stomatal conductance and intercellular CO2 concentration.

5.

UV-B

Coleus forskohlii

Indole acetic acid

Growth and morphology were adversely Takshak and Agrawal (2018) affected by reduction in protein and chlorophyll contents. IAA reversed the negative effect by alleviating the protein and chlorophyll content.

6.

UV radiation

Mentha aquatica L.

Manganese

Dry weight of root and shoot and the content of photosynthetic pigments were decreased. However, flavonoids, soluble carbohydrate, anthocyanins, MDA equivalents, hydrogen peroxide contents and the activity of antioxidant enzymes superoxide dismutase, catalase, and peroxidase were increased. Harmful effects were decreased upon Mn application.

7.

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TABLE 5.1 (Continued) S. Radiation no types

Model system

Mitigation strategies

Effect

References

Enterobacter cloacae

Protein profiling by SDS PAGE and 2Kumar et al. DE revealed major changes in the (2016) number as well as expression of proteins. Analysis of 2-DE gel spots indicated up/down-regulation of several proteins under the stress of UV-B radiation.

8.

β-Radiation

Lemna minor

Root fresh weight decreases and antioxidant defense system were increased to mitigate the oxidative stress inside the cell.

9.

μ-Radiation

Arachis hypogaea L.

Distortion of nuclear membrane, chloroplast swelling, thylakoid dilation, rupture of chloroplast outer membrane, and swollen endoplasmic reticulum were also noticed.

Sreedhar et al. (2013)

Nostoc commune

UV-B damages protein, breakdown of double stranded DNA, crosslink formation between DNA and protein and formation of cyclobutane dimers which negatively affect the DNA replication and protein formation.

Schulz and Scherer (1999)

10. UV-B

2-DE, Two-dimensional gel electrophoresis; MDA, malondialdehyde; CAT, catalase; IAA, indole acetic acid; PAGE, poly acrylamide gel electrophoresis; SDS, sodium dodecyl sulphate; SOD, superoxide dismutase.

been utilized to reconstruct variations in the light regime over time. Natural populations of the same species may vary in their concentration, indicating genetic differences. MAAs are water-soluble, substituted cyclohexenones which are linked to amino acids and aminoalcohols, and have absorption maxima between 310 and 360 nm. It probably originates from the first part of the shikimate pathway (Favre-Bonvin et al., 1987). Scytonemin is another pigment with UV-shielding properties found in cyanobacteria. It has an in vivo absorption maximum at 370 nm and is located in the cyanobacterial sheath. However, the damage to DNA was cured by photoreactivation at wavelengths from B395 450 nm. Typical ROS quenchers such as ascorbic acid, N-acetyl-L-cysteine, or sodium pyruvate have protective effects absence of ozone in the stratosphere (McKenzie et al., 2003). This stress signal is subsequently amplified and transmitted using cyclic nucleotides as secondary messengers followed by the production of shock proteins. In the terrestrial Nostoc commune species, UV-B treatment increased the concentration of 493 proteins out of 1350. In addition to direct UV-B-induced damage to the DNA, oxidative stress (singlet oxygen and superoxide radicals) and damage were reported, causing lipid peroxidation and DNA strand breakage. After prolonged UV-B exposures, an adaptation to the ROS stress has been observed. Typical ROS quenchers such as ascorbic acid, N-acetyl-L-cysteine or sodium pyruvate have protective effects.

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5.4.3 Ultraviolet-B as a protectant in plants Plants are unavoidably exposed to UV-B because they need to capture sunlight for photosynthesis. The fact that plants rarely display signs of UV damage in the natural environment demonstrates that they have evolved very effective mechanisms for UV protection and repair. The protective mechanisms include the deposition of UV-absorbing phenolic compounds in the outer epidermal tissues and the production of antioxidant systems. Repair of UV damage involves enzymes such as DNA photolyases. Furthermore, responses to UV-B modify the biochemical composition of plants, influence plant morphology, and help to deter pests and pathogens. It is well established that many plant responses to UV-B involve the regulation of gene expression. UV-B exposure stimulates the expression of hundreds of genes, including those involved in UV protection and repair. Low UV-B fluency rates (1 μmol m22 s21) cause no or very low amounts of CPDs that are below the limit of detection but stimulate protective and photomorphogenetic responses (Batschauer et al., 1996; Kim et al., 1998; Frohnmeyer et al., 1999) that affect the plant’s resistance to UV-B stress and other biotic stress types (Kim et al., 1998; Ballare, 2003). It is important to understand how plants respond to UV-B and determine the contribution of UV-B responses to normal plant growth and development. In fact, it will not be possible to obtain a complete understanding of the role of light in controlling plant development without knowledge of the regulatory effects of UV-B. Plants may also rapidly adjust their mechanism of UV protection in response to daily changes in UV irradiances. Protection against UVR increases from dawn to midday and then decreases toward sunset (Barnes et al., 2008). How plants achieve these rapid changes and what the significance is for function beyond protection from UVR is not yet known. Increased allocation of carbon to UV-absorbing compounds may divert carbon from growth and photosynthetic functions that reduce UV protection during times of the day when levels of UVR are low could enhance the daily gain of carbon (Sumbele et al., 2012). Much remains to be learnt about the cellular and molecular mechanisms of UV-B perception and signal transduction leading to the control of gene expression. Interestingly, exposure of plants to UV-B can also promote resistance to a variety of insect pests. Thus preexposure of plants to UV-B reduces subsequent feeding by insects and, conversely, filtering of UV-B from light sources makes leaf tissue more palatable to insects. The extent of resistance is dependent on both the plant and pest species. In several studies the protective effects of UV-B were correlated with changes in biochemical composition of leaf tissue that resembled the plant’s defense responses to insect attack. Hence there is overlap in the molecular responses activated by UV-B exposure and those triggered by wounding and insect herbivory.

5.4.4 Transduction of signal via ultraviolet damage UV-B can act as a signal to induce changes in gene expression at a distance from its origin of perception (Jordan, 1996). This perception mechanism for UV-B must then stimulate a signal transduction system through a series of intermediates that control/regulate the activity of genes. No specific photoreceptor molecule, however, has been identified that can perceive the UV-B signal. This is made more complex as the UV-B region of the spectrum is strongly absorbed by a wide range of biologically active molecules, such as nucleic

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acids, aromatic amino acids, lipids, and phenolic compounds. Thus a crucial question is how UV-B perceived and the response generated at the molecular level. In addition, the plant must also translate a number of other signals generated within the environment (different wavelengths of light, temperature, draught, pollutants, etc.) or by biotic factors (pathogens, symbionts, etc.). The signal transduction pathway(s) must therefore be able to recognize and differentiate between signals and interpret them prior to any response. Signal transduction pathways have been studied by Mackerness and Jordan (1999) and Mackerness et al. (1999). ROS increase in response to UV-B and are an important component in the regulation of both upregulated and downregulated genes. The nature and origin of the ROS involved in the early part of UV-B-induced signaling pathways have been investigated in A. thaliana. The increase in PR-1 transcript and decrease in Lhcb transcript in response to UV-B exposure was shown to be mediated through pathways involving hydrogen peroxide (H2O2) derived from superoxide (O2 2 ). In contrast, the upregulation of PDF1.2 transcript was mediated through a pathway involving O2 2 directly. The origins of the ROS were also shown to be distinct and to involve NADPH oxidase and peroxidase(s). The upregulation of Chs by UV-B was not affected by ROS scavengers but was reduced by inhibitors of nitric oxide synthase (NOS) or NO scavengers. Together these results suggest that UV-B exposure leads to the generation of ROS from multiple sources, and NO, through increased NOS activity, giving rise to parallel signaling pathways mediating responses of specific genes to UV-B radiation. In addition to the increase in ROS, other known signal transduction intermediates increase their levels. These include salicyclic acid (SA), jasmonic acid (JA), and ethylene using Arabidopsis mutants that are insensitive to SA, JA, and ethylene.

5.4.5 Plant hormones as protectants against harmful radiation Plant hormones are natural, endogenously produced compounds that show their active behavior at very low concentrations and promote growth and development as a regulatory molecule. These include auxins, cytokinins, gibberellins, and abscisic acid. Among all these, auxin is naturally occurring, and a physiologically active hormone. Auxins have been associated with UV-B based on different similarities between UV-B-acclimated plants and phytohormone mutants (Jansen, 2002). UVB can also mediate changes in the expression of auxin-related genes in seedlings as well as in mature leaves (Hectors et al., 2007; Vandenbussche et al., 2014). At distinct cellular level, auxin can be involved in the morphogenesis induced by UV-B and auxin homeostasis can be affected by various means, such as photooxidative damage, biosynthesis, conjugation, and/or degradation (Jansen et al., 2001). It is either regulated at the level of redistribution (via transport, influx, and efflux) or at the level of a potential signal crosstalk between auxin and various components of the light signaling pathway, changing auxin sensitivity (Cluis et al., 2004; Fierro et al., 2015). They brassinolids (BRs) are plant-specific steroidal hormones having the properties of promoting growth in nearly all phases of plant development (Peng-Zhu et al., 2013). It also mediates the crosstalk between UV-B and BR that affects defense signaling in plants. Interestingly, BRs have been suggested as regulators of plant defense (De Bruyne et al., 2014). In wild-type plants, protein PR-5 expression is clearly upregulated by UV-B, while BR-deficient cpd mutants do not show this induction (Savenstrand et al., 2004).

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UV-B can slightly alter the spectrophotometric characteristics of Gibberellic acid (GAs), yet without affecting their growth-promoting activities (Baltepe and Mert, 1974). Jasmonic acid (JA) is the simplest nontraditional plant hormone which has its varied effects and functions in regulating plant developmental processes. Jasmonate (JA) is a well-known hormone in the regulation of defense against herbivores and necrotrophs and also has a role in thigmomorphogenesis and wounding responses. JA absorbs very poorly in the UVB region of the spectrum. At high intensities, UV-B has been shown to increase the production of JA in Arabidopsis (Mackerness et al., 1999). Furthermore, as reported for other hormones, exogenous application of JAs can induce the tolerance of plants to various stresses (Singh and Shah, 2014; Kaya and Doganlar, 2016).

5.5 Conclusion Although many plant responses to UVR have been reported, complete mechanistic details of most of these responses have not been elucidated. It is evident that radiation plays a beneficiary as well as a devastating effect on the growth, development, physiology, and yield of plants. However, the response to radiation differs vastly among various plant species, varying with environmental cues. In recent years, the biochemical responses of plants to UVR have been studied intensively. UV-R plays a versatile role in the coevolution on earth during the Archean era. It has not just evolved the life on earth at the extremes of survival but also mediated a pathway in developing various morphological characteristics in cyanobacteria with response to UV. UV-R appears to exacerbate the impact of plant pathogens. How plants achieve these rapid changes and what the significance is for function beyond protection from UVR are yet to be explored.

References Akbal, A., Kiran, Y., Sahin, A., Turgut-Balik, D., Balik, H.H., 2012. Effects of electromagnetic waves emitted by mobile phones on germination, root growth and root tip cell mitotic division of Lens culinaris. Pol. J. Environ. Stud. 21, 23 29. Allen, D.J., McKee, I.F., Farage, P.K., Baker, N.R., 1997. Analysis of the limitation to CO2 assimilation on the exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ. 20, 633 640. Baker, N.R., Nogues, S., Allen, D.J., 1997. Photosynthesis and photoinhibition. In: Lumsden, P.J. (Ed.), Plants and UV-B: Responses to Environmental Change. Cambridge University Press, pp. 113 134. Ballare, C.L., 2003. Stress under the sun: spotlight on ultraviolet-B responses. Plant Physiol. 132, 1725 1727. Baltepe, S., Mert, H.H., 1974. Preliminary report on effects of ultraviolet radiation on gibberellic acid solutions. Phyton (Austria). 15, 259 263. Barnes, P.W., Flint, S.D., Slusser, J.R., Gao, W., Ryel, R.J., 2008. Diurnal changes in epidermal UV transmittance of plants in naturally high UV environments. Physiol. Plant. 133, 363 372. Bashri, G., Parihar, P., Singh, R., Singh, S., Singh, V.P., Prasad, S.M., 2017. Physiological and biochemical characterization of two Amaranthus species under Cr (VI) stress differing in Cr (VI) tolerance. Plant Physiol. Biochem. 108, 12 23. Batschauer, A., Rocoll, M., Kaiser, T., Nagatani, A., Furuya, M., Schafer, E., 1996. Blue and UV-A-light-regulated CHS expression in Arabidopsis independent of phytochrome A and phytochrome B. Plant J. 9, 63 69. Bornman, J.F., 1989. Target sites of UV-B radiation in photosynthesis of higher plants. J. Photochem. Photobiol. 4, 145 158.

Plant Life under Changing Environment

120

5. Plant responses to radiation stress and its adaptive mechanisms

Chauhan, Y.S., Katiyar, S.R., 1998. Effects of radiation and growth hormones on pollen germination, pollen tube growth and modulation of radiation responses of Pinus kesiya Royle ex Gord. Cytologia 63, 341 348. Cluis, C.P., Mouchel, C.F., Hardtke, C.S., 2004. The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J. 38, 332 347. Conde, F.R., Churio, M.S., Previtali, C.M., 2004. The deactivation pathways of the excited-states of the mycosporinelike amino acids shinorine and porphyra-334 in aqueous solution. Photochem. Photobiol. Sci. 3, 960 967. Dawson, A., 1992. Global Climate Change. Oxford University Press, UK, 48 p. De Bruyne, L., Hofte, M., De Vleesschauwer, D., 2014. Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Mol. Plant 7, 943 959. Dillon, J.G., Miller, S.R., Castenholz, R.W., 2003. UV-acclimation responses in natural populations of cyanobacteria (Calothrix sp.). Environ. Microbiol. 5, 473 483. Ehling-Schulz, M., Bilger, W., Scherer, S., 1997. UV-B induced synthesis of photoprotective pigments and extracellular polysaccharides in the terrestrial cyanobacterium Nostoc commune. J. Bacteriol. 179, 1940 1945. Favre-Bonvin, J., Bernillon, J., Salin, N., Arpin, N., 1987. Biosynthesis of mycosporines: mycosporine glutaminol in Trichothecium roseum. Phytochemistry 26, 2509 2514. Fierro, A.C., Leroux, O., De Coninck, B., Cammue, B.P.A., Marchal, K., Prinsen, E., et al., 2015. Ultraviolet-B radiation stimulates downward leaf curling in Arabidopsis thaliana. Plant Physiol. Biochem. 93, 9 17. FAO, 2009. Electronic Publishing Policy and Support Branch Communication Division. Food and Agriculture Organization of the United Nations, Rome. FAO, ISBN 978-92-5-106215-9. Frohnmeyer, H., Loyall, L., Blatt, M.R., Grabov, A., 1999. Millisecond UV-B irradiation evokes prolonged elevation of cytosolic-free Ca21 and stimulates gene expression in transgenic parsley cell cultures. Plant J. 20, 109 118. Fukuchi, K., Takahashi, Tatsumoto, H., 2004. Impacts of UV-A irradiation on laser-induced fluorescence spectra in UV-B damaged peanut (Arachishypogaea L.) leaves. Environ. Technol. 25, 1233 1240. Hader, D.P., Kumar, H.D., Smith, R.C., Worrest, R.C., 2007. Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem. Photobiol. Sci. 6, 267 285. Halliwell, B., Gutteridge, J.M.C., 1986. J. Pharma. Sci. 75 (1), 105 106. Hectors, K., Prinsen, E., De Coen, W., Jansen, M.A.K., Guisez, Y., 2007. Arabidopsis thaliana plants acclimated to low dose rates of ultraviolet B radiation show specific changes in morphology and gene expression in the absence of stress symptoms. New Phytol. 175, 255 270. Helbling, E.W., Gao, K., Ai, H., Ma, Z., Villafane, V.E., 2006. Differential responses of Nostoc sphaeroides and Arthrospira platensis to solar ultraviolet radiation exposure. J. Appl. Phycol. 18, 57 66. Hideg, E., Barta, C., Ka´lai, T., Vass, I., Hideg, K., Asada, K., 2002. Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol. 43, 1154 1164. Hidema, J., Teranishi, M., Iwamatsu, Y., 2005. Spontaneously occurring mutations in the cyclobutane pyrimidine dimer photolyase gene cause different sensitivities to ultraviolet-B in rice. Plant J. 43 (1), 57 67. Jansen, M.A.K., 2002. Ultraviolet-B radiation effects on plants: induction of morphogenic responses. Physiol. Plant. 116, 423 429. Jansen, M.A.K., Noort, R.E., Tan, M.Y.A., Prinsen, E., Lagrimini, L.M., Thorneley, R.N.F., 2001. Phenol-oxidizing peroxidases contribute to the protection of plants from ultraviolet radiation stress. Plant Physiol. 126, 1012 1023. Jiang, H., Qiu, B., 2005. Photosynthetic adaptation of a bloom forming cyanobacterium Microcystis aeruginosa (Cyanophyceae) to prolonged UV-B exposure. J. Phycol. 41, 983 992. John, C.F., Morris, K., Jordan, B.R., Thomas, B., Mackerness, A.H., 2001. Ultraviolet-B exposure leads to up-regulation of senescence-associated genes in Arabidopsis thaliana. J. Exp. Bot. 52 (359), 1367 1373. Jordan, B.R., 1996. The effects of ultraviolet-B radiation on plants: a molecular perspective. In: Callow), J.A. (Ed.), Advances in Botanical Research, vol. 22. Academic Press Ltd., pp. 97 162. Karentz, D., McEuen, F.S., Land, M.C., Dunlap, W.C., 1991. Survey of mycosporine like amino acid compounds in Antarctic marine organism: potential protection from ultraviolet exposure. Mar. Biol. 108, 157 166. Kaya, A., Doganlar, Z.B., 2016. Exogenous jasmonic acid induces stress tolerance in tobacco (Nicotiana tabacum) exposed to imazapic. Ecotoxicol. Environ. Saf. 124, 470 479. Kim, B.C., Tenessen, D., Last, R., 1998. UV-B induced photo-morphogenesis in Arabidopsis thaliana. Plant J. 15, 667 674. Korystov, Y.N., Narimanov, A.A., 1997. Biologia (Bratislava) 52, 121 124.

Plant Life under Changing Environment

References

121

Koti, S., Reddy, K.R., Reddy, V.R., Kakani, V.G., Zhao, D., 2005. Interactive effects of carbon dioxide, temperature, and ultraviolet-B radiation on soybean (Glycine max L.) flower and pollen morphology, pollen production, germination, and tube lengths. J. Exp. Bot. 56, 725 736. Kovacs, E., Keresztes, A., 2002. Effect of gamma and UV-B/C radiations on plant cells. Micron 33, 199 210. Kumagai, T., Sato, T., 1992. Inhibitory effects of increase in near-UV radiation on the growth of Japanese rice cultivars (Oryza sativa L.) in a phytotron and recovery by exposure to visible radiation. Jpn. J. Breed. 42, 545 552. Kumar, A., Tyagi, M.B., Jha, P.N., Srinivas, G., Singh, A., 2003. Inactivation of cyanobacterial nitrogenase after exposure to ultraviolet-B radiation. Curr. Microbiol. 46, 380 384. Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33 (7), 1870 1904. Liu, Z., Hader, D.P., Sommaruga, R., 2004. Occurrence of mycosporine-like amino acids (MAAs) in the bloomforming cyanobacterium Microcystis aeruginosa. J. Plankton Res. 26, 963 966. Mackerness, S.A.H., Jordan, B.R., 1999. Changes in gene expression in response to UV-B induced stress. In: Pessarakli, M. (Ed.), Handbook of Plant and Crop Stress. Marcel Dekker Inc, pp. 749 768. Mackerness, S., Surplus, S.L., Blake, P., John, C.F., Buchanan-Wollaston, V., Jordan, B.R., et al., 1999. Ultraviolet-Binduced stress and changes in gene expression in Arabidopsis thaliana: role of signaling pathways controlled by jasmonic acid, ethylene and reactive oxygen species. Plant Cell Environ. 22, 1413 1423. McCormick, J.F., Platt, R.B., 1962. Effects of ionizing radiation on a natural plant community. Radiat. Bot. 2, 161 188. McKenzie, R.L., Bjo¨rn, L.O., Bais, A., Ilyas, M., 2003. Changes in biologically active ultraviolet radiation reaching the Earth’s surface. Photochem. Photobiol. Sci. 2, 5 15. Mewis, I., Schreiner, M., Nguyen, C.N., Krumbein, A., Ulrichs, C., Marc Lohse, M., et al., 2012. UV-B irradiation changes specifically the secondary metabolite profile in broccoli sprouts: induced signaling overlaps with defense response to biotic stressors. Plant Cell Physiol. 53 (9), 1546 1560. Nawkar, G.M., Maibam, P., Park, J.H., Sahi, V.P., Lee, S.Y., Kang, C.H., 2013. UV-induced cell death in Plants. Int. J. Mol. Sci. 14, 1608 1628. Oliveira, J.M., Almeida, A.R., Pimentel, T., Andrade, T.S., Henriques, J.F., Soares, A.M., et al., 2016. Effect of chemical stress and ultraviolet radiation in the bacterial communities of zebrafish embryos. Environ. Pollut. (Barking, Essex: 1987 208 (Pt B), 626 636. Peng-Zhu, J.Y., Sae-Seaw, J., Wang, Z.Y., 2013. Brassinosteroid signaling. Development 140, 1615 1620. Pierson, B.K., Mitchell, H.K., Ruff-Roberts, A.L., 1993. Chloroflexus aurantiacus and ultraviolet radiation: implications for Archean shallow water stromatolites. Orig. Life Evol. Biosph. 23, 243 260. Rajagopal, S., Sicora, C., Va´rkonyi, Z., Musta´rdy, L., Mohanty, P., 2005. Protective effect of supplemental low intensity white light on ultraviolet-B exposure-induced impairment in cyanobacterium Spirulina platensis: formation of air vacuoles as a possible protective measure. Photosyn. Res. 85, 181 189. Rastogi, S.K., Pal, P., Aston, D.E., Bitterwolf, T.E., Branen, A.L., 2011. 8-Aminoquinoline functionalized silica nanoparticles: a fluorescent nanosensor for detection of divalent zinc in aqueous and in yeast cell suspension. ACS Appl. Mater Inter. 3 (5), 1731 1739. Sagan, L.A., 1987. Health Phys. 52, 521 525. Salter, L., Hewitt, C.N., 1992. Ozone-hydrocarbon interactions in plants. Photochemistry 31 (4), 4045 4050. Santos, J., Sousa, M.J., Leao, C., 2012. Ammonium is toxic for aging yeast cells, inducing death and shortening of the chronological lifespan. PLoS One 7 (5), e3709. Savenstrand, H., Brosche, M., Strid, A., 2004. Ultraviolet-B signalling: Arabidopsis brassinosteroid mutants are defective in UV-B regulated defence gene expression. Plant Physiol. Biochem. 42, 687 694. Scherer, S., Chen, T.W., Bosger, P., 1988. A new UV-A and B protecting pigment in the terrestrial cyanobacterium Nostoc commune. Plant Physiol. 88, 1055 1057. Schulz, M.E., Scherer, S., 1999. UV protection in cyanobacteria. Eur. J. Phycol. 34 (4), 329 338. Singh, I., Shah, K., 2014. Exogenous application of methyl jasmonate lowers the effect of cadmium-induced oxidative injury in rice seedlings. Phytochemistry 108, 57 66. Singh, M., Bashri, G., Prasad, S.M., 2019. Kinetin alleviates UV-B induced damage in Solanum lycopersicum: Implications of phenolics and antioxidants. J. Plant Growth Regul 1 11. Available from: https://doi.org/ 10.1007/s00344-018-9894-8. Sinha, R.P., Hader, D.P., 2003. Biochemistry of mycosporine-like amino acids (MAAs) synthesis: role in photoprotection. Recent Res. Dev. Biochem. 4, 971 983.

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122

5. Plant responses to radiation stress and its adaptive mechanisms

Sinha, R.P., Ambasht, N.K., Sinha, J.P., Hader, D.P., 2003. Wavelength-dependent induction of a mycosporine-like amino acid in a rice-field cyanobacterium, Nostoc commune: role of inhibitors and salt stress. Photochem. Photobiol. Sci. 2, 171 176. Sinha, R.P., Kumar, A., Tyagi, M.B., Hader, D.P., 2005. Ultraviolet-B induced destruction of phycobilin proteins in cyanobacteria. Mol. Biol. Plants 11, 313 319. Sreedhar, M., Chaturvedi, A., Aparna, M., Kumar, P.D., Singhal, R.K., Venu-Babu, P., 2013. Influence of γ-radiation stress on scavenging enzyme activity and cell ultra-structure in groundnut (Arachis hypogaea L.). Pelagia Research Library, Adv. App. Sci. Res. 4 (2), 35 44. Stefi, A.L., Margaritis, L.H., Christodoulakis, N.S., 2016. The effect of the non-ionizing radiation on cultivated plants of Arabidopsis thaliana (Col.). Flora 223, 114 120. Sumbele, S., Fotelli, M.N., Nikolopoulos, D., Tooulakou, G., Liakoura, V., Liakopoulos, G., et al., 2012. Photosynthetic capacity is negatively correlated with the concentration of leaf phenolic compounds across a range of different species. AoB Plants 2012, pls025. Takshak, S., Agrawal, B., 2018. Interactive effects of supplemental ultraviolet-B radiation and indole-3-acetic acid on Coleus forskohlii Briq. Alterations in morphological-, physiological-, and biochemical characteristics and essential oil content. Ecotoxicol. Environ. Saf. Available from: https://doi.org/10.1016/j.ecoenv.2017.08.059. Teramura, A.H., 1983. Effects of ultraviolet-B radiation on the growth and yield of crop plants. Physiol. Plant. 58 (3), 415 427. Teramura, A.H., 1987. Soybean growth to enhanced levels of ultraviolet radiation under greenhouse conditions. Am. J. Bot. 74 (7), 975 979. Teranishi, M., Taguchi, T., Ono, T., Hidema, J., 2012. Augmentation of CPD photolyase activity in japonica and indica rice increases their UV-B resistance but still leaves the difference in their sensitivities. Photochem. Photobiol. Sci. 11 (5), 812 820. Tevini, M., Braun, J., Fieser, G., 1991. The protective function of the epidermal layer of rye seedlings against ultraviolet-B radiation. Photochem. Photobiol. 53, 329 333. Vandenbussche, F., Tilbrook, K., Fierro, A.C., Marchal, K., Poelman, D., Vander, S.D., et al., 2014. Photoreceptor mediated bending towards UV-B in Arabidopsis. Mol. Plant 7, 1041 1052. White, A.L., Jahnke, L.S., 2002. Contrasting effects of UV-A and UV-B on photosynthesis and photo-protection of beta carotene in two Dunaliella sp. Plant Cell Physiol. 43 (8), 877. Wi, S.G., Chung, B.Y., Kim, J.S., Kim, J.H., Baek, M.H., Lee, J.W., et al., 2007. Effects of gamma irradiation on morphological changes and biological responses in plants. Micron 38, 553 564. Worrest, R.C., Smythe, K.D., Tait, A.M., 1989. Linkages between climate change and stratospheric ozone depletion. In: White, J.C. (Ed.), Global Climate Change Linkages, Acid Rain, Air Quality and Stratospheric Ozone. Elsevier Science Publishing Company, Inc., USA, pp. 67 78. Yadav, G., Srivastava, P.K., Parihar, P., Tiwari, S., Prasad, S.M., 2016. Oxygen toxicity and antioxidative responses in arsenic stressed Helianthus annuus L. seedlings against UV-B. J. Photochem. Photobiol. B: Biol. 165, 58 70. Yamamoto, A., Hirouchi, T., Mori, T., Teranishi, M., Hidema, J., Morioka, H., et al., 2007. Biochemical and biological properties of DNA photolyases derived from ultraviolet sensitive rice cultivars. Genes Genet. Syst. 82 (4), 311 319. Zlatev, S.Z., Lidon, J.C.F., Kaimakanova, M., 2012. Plant physiological responses to UV-B radiation. Emir. J. Food Agric. 24, 481 501.

Further reading Castenholz, R.W., 2004. Phototrophic bacteria under UV stress. In: Seckbach, J. (Ed.), Origins, Evolution and Biodiversity of Microbial Life. Kluwer Academic Publishers, Dordrecht, pp. 445 461. Haider, S.I., Johnell, K., Thorslund, M., Fastbom, J., 2007. Trends in polypharmacy and potential drug interactions across educational groups in elderly patients in Sweden for the period 1992 2002. Int. J. Clin. Pharmacol. Ther. 45 (12), 643 653. Teranishi, M., Iwamatsu, Y., Hidema, J., Kumagai, T., 2004. Ultraviolet-B sensitivities in Japanese lowland rice cultivars: cyclobutane pyrimidine dimer photolyase activity and gene mutation. Plant Cell Physiol. 45 (12), 1848 1856. Ulm, R., Nagy, F., 2005. Signaling and gene regulation in response to UV light. Curr. Opin. Plant Biol 8, 477 482.

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6 Regulation of low phosphate stress in plants Stanislaus Antony Ceasar1,2 1

Division of Plant Biotechnology, Entomology Research Institute, Loyola College, Chennai, India 2Functional Genomics and Plant Molecular Imaging Lab, University of Liege, Liege, Belgium

6.1 Introduction Phosphorous (P) serves many important cellular functions in many organisms including plants. It is crucial for the structure of nucleic acids, high-energy compounds, regulation of enzyme activities, and integrity of membranes. Deficiency of P in soil reduces the growth and yield in many crops, which is a major problem for food production worldwide (Baker et al., 2015). Plants uptake P from the soil in the form of inorganic phosphate (Pi); this process is influenced by soil pH (Schachtman et al., 1998). Most of the soil-bound Pi is also not readily accessible to plants due to its low mobility and high reactivity with cations [iron (Fe) and aluminum (Al)] at acid soils, with calcium (Ca) at alkaline soils (Raghothama, 1999). Therefore application of external synthetic P fertilizers has become a routine practice to improve the crop yields in agricultural systems. The phosphate fertilizers are obtained by mining of natural rock phosphate reserves. Rock phosphate reserves are not evenly spread throughout the world; moreover, the available reserves are also expected to get exhausted in the next 100 years or soon (Cordell et al., 2009). It is estimated that farmers, for excessive production, often apply too much of synthetic phosphate fertilizers, and its over use in farm lands causes environmental problems associated with eutrophication (Mekonnen and Hoekstra, 2018). So understanding the mechanism of Pi transport and regulatory mechanism of low Pi stress responses will help to improve the crop yields under Pi-deficient soils. At morphological, physiological, biochemical, and molecular levels, plants have diverse adaptive mechanisms to overcome the low Pi stress. Scores of reports are available on the studies related to low Pi-starvation responses of plants (Lo´pez-Arredondo et al., 2014). At

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morphological level, plants change their root system architecture (RSA) due to low Pi stress response. In addition, enhanced production of lateral roots and root hairs is seen while the growth of primary root is inhibited, by low Pi stress. At molecular level, plants express phosphate transporter genes at roots for the enhanced uptake of Pi from soil solution (Ceasar et al., 2017; Baker et al., 2015). Even several microRNAs (miRNAs) have also been found to be involved in long-distance signaling events during low Pi stress (Liu et al., 2014a). Apart from that, several transcription factors (TFs) have also been found to play key roles to regulate the low Pi stress response (Liang et al., 2014). Plants also produce and secrete several organic exudates and enzymes from roots to release the Pi from fixed compounds (Panigrahy et al., 2009). All these changes are helpful to overcome the low Pi stress in plants. As the ever-increasing world population is constantly putting more pressure on food production, we need to improve the sustainable production of food with limited use of synthetic fertilizers (Ceasar, 2018). Improving P-use efficiency (PUE) of crop plants that is combined by P-acquisition efficiency (PAE) and P-utilization efficiency (PUtE) is essential for improving the crop production without the use of synthetic P fertilizers (Maharajan et al., 2018). It is essential as the P rock reserves are depleting rapidly, and limited use of P fertilizers will also be helpful for the sustainable food production. Overall, it will ensure the food security by conserving the environment in future.

6.2 Morphological responses under low inorganic phosphate stress 6.2.1 Changes in root system architecture Root is the primary and most important organ of plants for accessing water and nutrients from the soil solutions. The RSA changes in response to the nutrient and water levels. Plants alter their RSA due to Pi stress and produce a modified shallower root system. The modification of RSA is more potent trait for the production of crop plants with improved PAE (Lynch and Brown, 2008; Rouached et al., 2010; Pe´ret et al., 2011). The plants modify the RSA to suit with the topsoil foraging under low Pi-stress conditions. Usually, topsoil layers have higher Pi content when compared to lower subsoil layers due to the deposition of plant residues over the time (Pe´ret et al., 2014). Therefore this modification will help to improve topsoil foraging at low Pi stress (Ham et al., 2018). The changes in RSA of foxtail millet plants grown under the soils with different levels of Pi are shown in Fig. 6.1. In order to increase the shallow root system under low Pi stress, plants also modify their growth angles. It has been proved that growth angles have been modified by low Pi stress with shallower growth angles in maize (Zea mays) (Zhu et al., 2005) and bean (Phaseolus vulgaris) (Liao et al., 2004). Plants also produce adventitious roots from subterranean shoot tissue under low Pi soils to increase the topsoil foraging (Lynch and Ho, 2005). Plants also produce more lateral roots with increased lateral branches that also help to increase the topsoil foraging in maize (Zhu and Lynch, 2004). It has also been documented that plants also induce more root hairs under low Pi soils, and the trait is directly related to the increased Pi uptake (Fig. 6.1). The higher number of root hairs helped to improve the root absorption capacity under low Pi soils. In many plants, Pi uptake is correlated

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FIGURE 6.1 Modification of RSA under low Pi stress in foxtail millet. RSA of 2-month-old foxtail millet plants grown under low and high Pi conditions are shown. The main pictures show the modification of primary and lateral roots by Pi levels. The inset pictures show the root hair induction based on the levels of external Pi supply. Pi, Inorganic phosphate; RSA, root system architecture.

with both number and length of root hairs under low Pi condition including in soybean (Glycine max) (Vandamme et al., 2013) and beans (Yan et al., 2004). Low Pi stress
induced modifications of RSA, such as inhibition of primary root growth, proliferation lateral roots, and root hairs, were seen in many plants (Dinkelaker et al., 1995; Carswell et al., 1996; Borch et al., 1999; Kim et al., 2008; Lambers et al., 2011; Jin et al., 2012). These modifications are helpful for topsoil foraging under low Pi-stress condition.

6.2.2 Mechanism of root system architecture modification under low inorganic phosphate stress condition 6.2.2.1 Mechanism of changes in primary root growth Recent studies shed more light on molecular mechanism involved in changes of RSA under low Pi-stress conditions. The mechanism of inhibition of primary root growth by low Pi stress is controlled by many genes. It has been proved that low Pi stress is a major factor controlling the primary root (PR) length when compared to the effect of deficiencies of other nutrients (Gruber et al., 2013; Kellermeier et al., 2014). LOW PHOSPHATE ROOT1 (LPR1) and LPR2 that produce multicopper oxidases (Svistoonoff et al., 2007) and PHOSPHATE DEFICIENCY RESPONSE2 (PDR2) that produces a P-type 5 ATPase (Ticconi et al., 2009) are responsible for controlling the primary root growth (Pe´ret et al., 2014). PDR2 is an endoplasmic reticulum (ER)-related protein; it is required for the proper expression of SCARECROW which is involved in the patterning and stem-cell maintenance of roots under low Pi-stress condition. Under low Pi stress, both PDR2 and LPR1 function in an ER-resident pathway to adjust the root meristem activity (Pe´ret et al., 2014). ALTERED PHOSPHATE STARVATION RESPONSE1 (APSR1) is a key player for the maintenance of root meristem (Gonza´lez-Mendoza et al., 2013). APSR1 is highly expressed under replete Pi than under deplete Pi condition. So APSR1 has also been proposed to be necessary for reducing the primary root growth under low Pi-stress condition.

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6.2.2.2 Mechanism of changes in lateral root growth Auxin is a key player for modulating the lateral root formation at low Pi-stress conditions (Pe´ret et al., 2014). Under low Pi stress, increased sensitivity of auxin triggers the initiation and emergence of more lateral roots. It has been reported in Arabidopsis thaliana that TRANSPORT INHIBITOR RESPONSE1 (TIR1) acts as an auxin receptor and is responsible for the induction of lateral roots; expression of TIR1 was increased under low Pistress condition when compared to normal Pi supply (Pe´rez-Torres et al., 2008). Proliferation of lateral roots mediated by TIR1 in response to low Pi stress also requires the presence of TFs Auxin Response Factor (ARF) 7 (ARF7) and ARF19 TFs (Pe´rez-Torres et al., 2008). Expansins involved in the control of cell division and expansion also modulate the RSA under low Pi-stress condition (Guo et al., 2011). Overexpression of soybean β-expansin (GmEXB2) in A. thaliana had positive effect with higher cell division (69%) and elongation (53%) in root with 170% more growth and 20% higher Pi uptake under both levels of Pi (Guo et al., 2011). Even PDR2 discussed earlier has also proved to be involved in the development of lateral roots under low Pi-stress condition (Ticconi et al., 2009). In rice a major quantitative trait locus (QTL) controlling low Pi tolerance is PHOSPHORUS UPTAKE 1 that encodes a gene PHOSPHORUS STARVATION TOLERANCE1, which is also a regulator of RSA under low Pi (Gamuyao et al., 2012). 6.2.2.3 Mechanism of changes in root hairs The key molecular events involved in root hair development under low Pi stress have been reported in recent years. Root hair production has proved to be regulated by the TFs ROOT HAIR DEFECTIVE-LIKE1 (RSL1) and RSL2 (Secco et al., 2014). Especially, according to a recent study, the root hair length is critically maintained by RSL4 (Datta et al., 2015). LRL genes are the key players of root hair changes (Tam et al., 2015) and are essential for low Pi-stress tolerance in rice (Yi et al., 2005). Root hair changes are also regulated by phosphoinositides with a phosphorylated inositol head group, which play major roles in low Pi stress responses (Xue et al., 2009). For example, phosphatidylinositol 3-phosphate [PtdIns(3) P] is important for root hair elongation in A. thaliana (Lee et al., 2008). ATF WRKY6 is also found to regulate the root hair density in A. thaliana under low Pi condition (Stetter et al., 2017). More recently, it has been reported that RSL2 genes could improve the root hair production and for an example, overexpression of Brachypodium distachyon (Bd) BdRSL2 and BdRSL3 genes increased the root hair length threefold (Zhang et al., 2018).

6.3 Molecular responses to low phosphate stress 6.3.1 Induction of phosphate transporter genes by low inorganic phosphate stress Phosphate transporters play key roles in the movement of Pi under low Pi stress. These transporters mediate the uptake of Pi from soil solutions, translocation into shoot by xylem loading, and sequestration of Pi into organelles such as chloroplast, mitochondria, and vacuoles (Fig. 6.2). The key transporters identified so far include Phosphate Transporter1 (PHT1), PHT2, PHT3, PHT4, and PHT5. These transporters also function to maintain the

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FIGURE 6.2 Site of localization of various phosphate transporters in a plant cell. The details on the site of action of each family of phosphate transporter with their direction of Pi transport are indicated. The PHT1 family transporters are involved with cellular uptake of Pi from soil solutions across the plasma membrane. PHT2s are found to be located at chloroplast membrane and involved with influx of Pi from cytosol into chloroplast matrix. PHT3s are mitochondria-specific transporters involved in traffic of Pi into mitochondrial matrix. PHT4s are found to mediate the Pi transport from cytosol to chloroplast matrix and also on the membranes of thylakoid. PHT5/ VPT1 family is vacuolar-specific transporter involved in import of Pi into vacuoles. SPX-MFS1 and SPX-MFS3 are also vacuolar-specific transporters with opposite traffic of Pi movement between cytosol and vacuoles. PHO1s are Pi exporters involved in xylem loading of Pi for export to shoot. PHT1, Phosphate Transporter1; Pi, inorganic phosphate.

Pi homeostasis under low Pi stress. The details of each of these transporters are discussed in detail in the following subsections. 6.3.1.1 Phosphate Transporter1 Plasma membrane
bound PHT1 family transporters are the primary channels of entry of Pi from solutions to the plant (Nussaume et al., 2011). Pi transport process is affected by soil pH as it can change the predominant forms of available Pi (HPO22 or H2 PO2 4 4) (Schachtman et al., 1998). PHT1 family transporters were first identified and characterized in A. thaliana (Muchhal et al., 1996). Subsequently, PHT1 members have been characterized in several plants, namely, rice, maize, barley, tomato, potato, Madagascar periwinkle, white lupin, barrel medic, tobacco, wheat, and foxtail millet (reviewed by Nussaume et al., 2011; Baker et al., 2015). Each plant has a family of PHT1 genes, A. thaliana contains 9 PHT1 genes, rice has 13, soybean has 14, and barley and foxtail millet contain 12 genes each (reviewed in Baker et al., 2015). Various members of the PHT1 genes exhibit dynamic patterns of expression with respect to site (tissue) and concentration of Pi (reviewed in Nussaume et al., 2011). These transporters were predominantly expressed in roots, epidermal cells, and the outer cortex of the root hair (Xiao et al., 2006; Misson et al., 2004). Localization studies have revealed that PHT1 is primarily targeted to the plasma membrane

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(Preuss et al., 2011). Some PHT1 transporters are also expressed in aerial parts of the plants involving in the remobilization of Pi from older tissues (Nussaume et al., 2011). PHT1 transporters show varied affinities from low (mM) to high (μM) range for Pi in the complementation experiments with yeast or Xenopus oocytes. For example, the affinity values of different transporters are 3.1 μM for A. thaliana AtPHT1;1 (Mitsukawa et al., 1997), 9.06 μM for barley HvPHT1;1 and 385 μM for HvPHT1;6 (Rae et al., 2003), 192 μM for Medicago truncatula MtPHT1;1 (Liu et al., 1998a), 23 μM for rice OsPHT1;8 (Jia et al., 2011), and 97 μM for rice OsPHT1;6 (Ai et al., 2009). However, other transporters such as OsPHT1;2 showed low affinity in the mM range, upon expression in Xenopus oocytes (Ai et al., 2009). However, a recent study also revealed that plant PHT1 transporters might have dual affinity which might be regulated by posttranslational modifications (Ayadi et al., 2015). Several PHT1 genes are induced under low Pi stress condition in many plants (Table 6.1). For example, transcripts OsPHT1;2, 1;6 were found in roots of 21-day-old rice seedlings grown without Pi (Ai et al., 2009) and OsPHT1;8 in 21-day-old seedlings under 1.5 μM Pi (Jia et al., 2011). Eight transcripts (AtPHT1;1, 1;2, 1;3, 1;4, 1;5, 1;7, 1;8, and 1;9) were found in roots of 21-day-old seedlings of A. thaliana grown under deplete Pi (Mudge et al., 2002), six transcripts (GmPHT1;1, GmPHT1;2, 1;5, 1;7, 1;10, and 1;12) were found in 21-day-old root of soybean seedlings grown under 10 μM Pi (Fan et al., 2013), and three transcripts (HvPHT1;1, 1;6, and 1;9) were found in roots of 16-day-old seedlings of barley grown under deplete Pi (7.7 mg per pot) (Huang et al., 2011). In addition, transcripts of ZmPHT1;1
1;5 were found in the root of maize grown under 10 μM Pi condition (Nagy et al., 2006). It was reported that OsPHT1;9 and 1;10 were identified in root tissues (root hairs and lateral roots) of 30day-old rice seedlings grown under low Pi condition (Wang et al., 2014c). Recently, four transcripts (OsPHT1;1, OsPHT1;2, OsPHT1;4, and OsPHT1;8) were found in IR64, Black Gora, and DJ123 genotypes of rice at low Pi (Julia et al., 2018). PHT1 proteins are delivered to the plasma membrane by PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 through an endomembrane-mediated delivery process (Chen et al., 2015). At sufficient Pi condition the PHT1 proteins are phosphorylated, which enhances the vacuolar delivery and subsequent degradation, and are dephosphorylated under low Pi conditions (Chen et al., 2015). Some PHT1 genes are also found to be specifically induced by arbuscular mycorrhizae fungal (AMF), and these details are discussed under a separate section on AMF. 6.3.1.1.1 Structural insights of Phosphate Transporter1 transporters

Out of other transporters, PHT1s are the most frequently studied; these belong to the major facilitator superfamily (MFS) of proteins and are Pi and H1 symporters. The PHT1 transporters contain 12 transmembrane alpha helices as like other MFS and are divided into two domains, N and C, each having 6 transmembrane helices (Karandashov et al., 2004; Ceasar et al., 2016). The first crystal structure of a eukaryotic fungal (Piriformospora ˚ (Pedersen et al., 2013); Pi binding indica) phosphate transporter (PiPT) was solved to 2.9 A site is located between the N and C domains and buried inside the membrane. The residues involved in the binding and transport of Pi and H1 and mechanism of Pi and H1 transport were also proposed in this study (Pedersen et al., 2013). The binding of Pi in PiPT is coordinated by Tyr 150, Gln 177, Trp 320, Asp 324, Tyr 328, and Asn 431, which are proposed to form H-bonding interactions with Pi as well as by electrostatic interaction from the edge of Phe 174 (Pedersen et al., 2013).

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TABLE 6.1 The Phosphate Transporter1 (PHT1) genes induced by low Pi stress in various plants. Name of the PHT1 gene

Plant

Affinity Site of induction by low Pi Reference

AtPHT1;1

Arabidopsis

High affinity




Mitsukawa et al. (1997)

AtPHT1;7, AtPHT 1;8, AtPHT1;9

Arabidopsis




Root

Mudge et al. (2002)

CfPHT1;1CfPHT1;2 CfPHT1;3 CfPHT1;4 CfPHT1;5

Cayenne pepper


Only in AMF inoculated roots

Chen et al. (2007a)

GmPHT1;1
GmPHT1;12

Soybean




Root

Fan et al. (2013)

GmPHT1;1, GmPHT1;2, GmPHT1;5, GmPHT1;7, and GmPHT1;10

Soybean

High affinity

Root

Fan et al. (2013)

HvPHT1;1

Barley

High affinity

Root

Rae et al. (2003)

HvPHT1;6

Barley

Low affinity

Moderately induced in root and shoot

Rae et al. (2003)

HvPHT1;9

Barley




Roots

Huang et al. (2011)

MtPHT1;1

Barrel medic

Low affinity




Liu et al. (1998b)

OsPHT1;2 OsPHT1;6

Rice

Low affinity




Ai et al. (2009)

OSPHT1;4

Rice




Root and shoot

Ye et al. (2015)

OsPHT1;8

Rice

High affinity

Root

Jia et al. (2011)

OsPHT1;8

Rice

High affinity

Shoot

Secco et al. (2013)

OsPHT1;9 and OsPHT1;10

Rice

High affinity

Root

Wang et al. (2014c)

OsPHT1;13

Rice




Root

Glassop et al. (2007)

PtaPHT1;1 PtaPHT1;2 PtaPHT1;3 PtaPHT1;7

Hardy orange




Roots

Shu et al. (2012)

PvPHT1;2

Kidney bean




Roots

Tian et al. (2007) (Continued)

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TABLE 6.1 (Continued) Name of the PHT1 gene

Plant

Affinity Site of induction by low Pi Reference

SiPHT1;2

Foxtail millet




Leaf

Ceasar et al. (2014)

SiPHT1;4

Foxtail millet




Root

Ceasar et al. (2014)

LePHT1;1 LePHT1;2

Tomato




Roots

Liu et al. (1998a)

SmPHT1;1 SmPHT1;2 SmPHT1;3 SmPHT1;4 SmPHT1;5

Eggplant




Leaf and roots

Chen et al. (2007a)

StPHT1;2

Potato

Low affinity

Roots

Leggewie et al. (1997)

ZmPHT1;1 ZmPHT1;2

Maize




Root and leaf:

Nagy et al. (2006)

ZmPHT1;3

ZmPHT1;1 ZmPHT1;2 All parts

ZmPHT1;6

Old leaves

Nagy et al. (2006)

Nagy et al. (2006)

TaPHT1;3, TaPHT1;6, and TaPHT1;8

Wheat




Root and shoot

Teng et al. (2017)

HvPHT1;1, HvPHT1;2, HvPHT1;3, and HvPHT1;4

Barley




Root

Glassop et al. (2005)

TaPHT1;2

Wheat

High affinity

Root

Guo et al. (2014)

LjPHT1;4

Lotus japonicas




Root

Volpe et al. (2016)

MtPHT1;4

Medicago truncatula

Root

Volpe et al. (2016)

ZmPHT1;2, ZmPHT1;3, ZmPHT1;4, Maize ZmPHT1;5, ZmPHT1;6, ZmPHT1;7, ZmPHT1;8, ZmPHT1;9, ZmPHT1;10, ZmPHT1;11, ZmPHT1;12, and ZmPHT1;13




Root

Liu et al. (2016a)

OsPHT1;1, OsPHT1;2, OsPHT1;4, and OsPHT1;8

Rice




Root

Julia et al. (2018)

TaPHT1;1, TaPHT1;2, TaPHT1;6, TaPHT1;8, TaPHT1;10, and TaPHT1;11

Wheat




Root

Gru¨n et al. (2018) (Continued)

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TABLE 6.1 (Continued) Name of the PHT1 gene

Plant

Affinity Site of induction by low Pi Reference

PvPht1;1, PvPht1;2, and PvPht1;3

Pteris vittata

High affinity




DiTusa et al. (2016)

GmPht1;1

Soybean




Young, mature, and old leaf, lateral, and main root

Song et al. (2014)

CmPht1;1

Chrysanthemum High affinity

Root

Liu et al. (2014b)

CmPht1;2

Chrysanthemum


Root

Liu et al. (2018a)

LePht1;1, LePht1;2, LePht1;3, LePht1;5, LePht1;6, and LePht1;7

Tomato




Root, stem, young leaves, flowers, fruits, fruits at green, and ripe fruits

Chen et al. (2014)

PvPHT1;2

Pteris vittata




Root and leaves

Cao et al. (2018)

MdPHT1;1, MdPHT1;2, MdPHT1;7, MdPHT1;11, and MdPHT1;12

Apple




Leaves and root

Sun et al. (2017)

StPHT1;1, StPHT1;4, and StPHT1;5

Potato




Leaf

Liu et al. (2017)

Root

Liu et al. (2017)

StPHT1;4, StPHT1;7, and StPHT1;8 EcPHT1;1, EcPHT1;3, and EcPHT1;4

Finger millet




Root and leaf

Pudake et al. (2017)

GhPHT1;5, GhPHT1;7, GhPHT1;14, and GhPHT1;16

Cotton




Root

Chao et al. (2017)

The PHT1s genes reported to be expressed are listed. Name of the host plant, site of expression, and affinities of the known transporters are listed with respective reference. AMF, Arbuscular mycorrhizae fungi.

Modeling of plant PHT1s based on fungal PiPT has been carried out to examine the putative Pi binding site across PHT1 family and their function (Ceasar et al., 2016). A homology model and Pi binding site of foxtail millet SiPHT1;2 is shown in Fig. 6.3. The phosphate binding site residues are well conserved among many plant PHT1 proteins and the P. indica protein (Ceasar et al., 2016). Even plant PHT1s with varying affinities and induction by AMF etc. all seem to possess conserved Pi binding site residues. So apart from amino acid residues involved in Pi and H1 binding and transport, affinity may be regulated by posttranslational modifications of PHT1s (Ceasar et al., 2016). 6.3.1.2 Phosphate Transporter2 Several transporters are also found to be localized on the membranes of intracellular organelles mediating Pi traffic between cytoplasm and these organelles. PHT2 has been found to be plastid-specific transporter and has high level of homology to Na1/Pi transporters of fungi

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FIGURE 6.3 Homology models of foxtail millet PHT1 transporter. (A) Whole model of SiPHT1;2 transporter with bound Pi molecule; (B) magnified view of Pi-binding amino acid residues of SiPHT1;2 transporter. The homology models were created using the determined structure of a high-affinity fungal PiPT as template (UniProt id: A8N031). The homology model of SiPHT1;2 was generated using Modeller v9.15 (Eswar et al., 2001), which created 100 models and 5 best models were chosen for further analysis. These models were analyzed using MolProbity (http://molprobity.biochem.duke.edu/) program, and Ramachandran plots were generated with the best model chosen based on the percentage residues in the favored and allowed regions and number of outliers. The model was viewed in PyMOL (https://www.pymol.org/) and analyzed for the Pi binding site residues. PHT1, Phosphate Transporter1; PiPT, Piriformospora indica phosphate transporter.

and mammals (Daram et al., 1999; Rausch and Bucher, 2002). It has been proved using a PHT2;1
GFP fusion that it is localized in the inner envelope of chloroplast, and Pi transport property was confirmed in yeast by heterologous expression (Versaw and Harrison, 2002). In rice a similar transporter (OsPHT2;1) has been found to be expressed in green tissues only with the induction of expression by low Pi stress (Shi et al., 2013). Leaf-specific expression of PHT2 genes was confirmed in pepper, eggplant, and tobacco under Glomus intraradices colonization (Chen et al., 2007a). Similarly, chloroplast-specific PHT2 was also identified and characterized in M. truncatula (MtPHT2;1) (Zhao et al., 2003). MtPHT2;1 was found to be specific for green tissues with expressions levels influenced by the light, development, and Pi status. 6.3.1.3 Phosphate Transporter3 The PHT3 members are localized in the membrane of mitochondria and involved in Pi exchange between cytosol and mitochondrial matrix. The uptake of Pi into the mitochondrial

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matrix is essential as ATP production is mediated by Pi through oxidative phosphorylation of ADP (Takabatake et al., 1999). These transporters contain six transmembrane domains and are highly conserved in the mitochondrial transporter family. PHT3 transporters were first identified and characterized during 1999 in soybean, maize, rice, and A. thaliana (Takabatake et al., 1999). Following this, PHT3 members have been identified in Lotus japonicas (Nakamori et al., 2002), soybean (Sha et al., 2014), wheat (Shukla et al., 2016), and poplar (Populus trichocarpa) (Zhang et al., 2016). Pi transport function of AtPHT3;2 and AtPHT3;3 were characterized by heterologous expression in Saccharomyces cerevisiae Δmir1Δpic2 mutant defective in mitochondrial Pi transport. PHT3 members of plants also proved to play key roles in stress signaling, growth, and seed maturation. For example, PHT3s were induced by high salinity in A. thaliana and AtPHT3 overexpressing plants were more sensitive to salt stress when compared with the wild-type (WT) plants at germination and seedling maturation stages (Zhu et al., 2012). Similarly, in poplar (P. trichocarpa), drought stress regulates the expression of PtPHT3;2b and PtPHT3;3b (Zhang et al., 2016). Similarly, overexpression of AtPHT3; 1 in A. thaliana hampers plant development by aborting the function of mitochondria (Jia et al., 2015). In wheat, TaPHT3 is a key player in grain development with tissue-specific expression of TaPHT3;1 (embryo and rachis) and TaPHT3;2 (aleurone) (Shukla et al., 2016). 6.3.1.4 Phosphate Transporter4 PHT4 transporters mediate the transport of Pi into chloroplasts, Golgi apparatus, and non photosynthetic plastids. PHT4 members were first identified and functions characterized in A. thaliana (Guo et al., 2008). These transporters are similar to solute carrier family sodium-dependent (SLC17) Type I Pi transporters. In A. thaliana, six members of PHT4 gene were identified and function characterized in yeast and in planta (Guo et al., 2008). Many PHT4 members have also been identified in other plants such as seven members in ´ ´ rice (Młodzinska and Zboinska, 2016), six in wheat (Shukla et al., 2016), and eight in P. trichocarpa (Zhang et al., 2016). However, apart from A. thaliana PHT4, members of other plants are yet to be studied in detail for function, localization, and transport activity. More distinct role of PHT4 member has also been elucidated in a recent study. In watermelon, ClPHT4;2 has been found to be involved in carotenoid contents and down-regulation of ClPHT4;2 reduced the carotenoid accumulation in fruits (Zhang et al., 2017). Further analysis revealed that ClPHT4;2 functions as a chromoplast-localized Pi transporter and can complement the phosphate-uptake-defective yeast mutant (Zhang et al., 2017). ClPHT4;2, a first member of this family, is proved to be involved in carotenoid accumulation. Members of PHT4 are also believed to regulate stress responses in other plants. In P. trichocarpa, expression of PtPHT4 members are regulated by Pi levels, PtPHT4;1a was induced by low Pi, and PtPHT4;1b and PtPHT4;5b were overexpressed under replete Pi (Zhang et al., 2016). In wheat, these members found to be involved in seed development; TaPHT4;2 and TaPHT4;4 were highly induced in endosperm at grain development stage (Shukla et al., 2016). In rice, all the PHT4 members were shown to be expressed in all tissues of seed (endosperm, vascular bundle/aleurone, and embryo) (Wang et al., 2016). In polar, PtPHT4;4 and PtPHT4;6 were highly expressed under high Pi condition and by drought stress (Zhang et al., 2016). In A. thaliana, PHT4;2 was known to contribute to Pi transport in isolated root plastids (Irigoyen et al., 2011). Starch synthesis was inhibited by excess Pi in the roots of pht4;2

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mutants due to defect in Pi export; this has altered expression patterns of starch synthesis genes and other genes of plastid transporter (Irigoyen et al., 2011). The PHT4;1 gene conferred defense response in A. thaliana and overexpression of PHT4;1 gene in WT plants conferred enhanced susceptibility to Pseudomonas infection (Wang et al., 2011a). PHT4;6 found to mediate the saline tolerance in A. thaliana seedlings and pht4;6 mutants had reduced primary root growth with higher branching of lateral roots (Cubero et al., 2009). PHT4;6 localized to the Golgi membrane and mediate the selective transport of Pi while preventing other anions. PHT4;6 also believed to be helpful for salt tolerance through Nglycosylation and cell wall synthesis (Cubero et al., 2009). 6.3.1.5 Phosphate Transporter5; vacuolar inorganic phosphate transporter1 The vacuole is the major Pi storage compartment in plant cells, and it plays an important role in Pi sequestration. Excess Pi is stored in the vacuole during sufficient Pi conditions and released from vacuole under low Pi conditions (Shane et al., 2004). A transporter specific to vacuole has been found to mediate the Pi transport into vacuole to maintain the Pi homeostasis (Bucher and Fabianska, 2016). The tonoplast-specific phosphate transporter was first identified by two independent groups first in A. thaliana (Liu et al., 2016b; Liu et al., 2015) and later in rice (Wang and Yue, 2015). In the very first report, it was mentioned as vacuolar phosphate transporter 1 (VPT1). VPT1 was primarily expressed in younger tissues confirming the function in Pi storage in young tissues and detoxification in older tissues (Liu et al., 2015). The vpt1 mutants looked short with less Pi storage than WT plants under high Pi conditions and knockdown of VPT1 caused the plants hypersensitive to both levels of Pi, thereby hampering the adaptability of plants to external Pi supply. The patch-clamp analysis using isolated vacuoles revealed that vpt1 could not show high Pi influx as in WT plants (Liu et al., 2015). Another closely timed study also reported the identification of A. thaliana VPT in the name of PHT5 (Liu et al., 2016b). It has been demonstrated that pht5;1 mutants accumulated less Pi and showed a lower vacuolar: cytoplasmic Pi ratio than WT plants. But overexpression of PHT5 caused massive Pi transport into vacuoles and altered the expression of Pi starvation responsive genes. It was also proved that overexpression of the rice OsSPX-MFS1 transports Pi in yeast vacuoles (Liu et al., 2016b). Similarly, in rice three SPX-MFS proteins (OsSPX-MFS1, OsSPX-MFS2, and OsSPX-MFS3) were reported (Wang and Yue, 2015); these were localized in the tonoplast. Among these three transporters, OsSPX-MFS3 could complement the yeast mutant ey917 to some degrees under sufficient Pi condition. OsSPX-MFS3 was able to mediate the influx or efflux of Pi based on external Pi concentrations in oocytes. However, in yeast and oocytes, OsSPX-MFS3 was found in the plasma membrane rather than tonoplast as in plant cells (Wang and Yue, 2015). However, the possibility of OsSPX-MFS3 involving in vacuolar Pi transport cannot be ruled out and needs further analysis. The identification and transport activity of all these transporters proved that transporters found on vacuolar membranes play important roles for homeostats of internal Pi levels by exchange of Pi in vacuoles. These transporters play key roles in the control of low Pi stress in plants. However, these are identified and characterized only in model plants so far, namely, A. thaliana and rice. Further research on these transporters especially with orphan crops such as millets will help to better understand the complex system of Pi transport and will help to enhance the PUE.

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6.3.2 PHOSPHATE1; the inorganic phosphate exporter A phosphate transporter family is also involved in the root-to-shoot movement of Pi based on the external Pi supply. The Pi is exported from root to aerial parts of the plants by xylem loading which is mediated by PHOSPHATE1 (PHO1) transporter family (Poirier et al., 1991; Arpat et al., 2012; Hamburger et al., 2002). PHO1 proteins belong to SPX
EXS subfamily and are involved in Pi export to shoots (Secco et al., 2012). The structure of PHO1 consists of a large cytoplasmic N-terminus with tripartite SPX domain, six transmembrane alpha helices, and cytoplasmic C-terminus with EXS domain (Wang et al., 2004). It has been proved that the EXS domain is essential for the functioning of PHO1 and is also involved in Pi signaling and transport activity of whole PHO1 (Wege et al., 2016). Like PHT1 family, each plant also seems to possess several members of PHO1 transporters. Ten members of PHO1 (PHO1;H1 to PHO1;H10) have been identified in A. thaliana, and three members are found with rice (OsPHO1;1, 1;2, ´ ´ and 1;3) (Młodzinska and Zboinska, 2016). In A. thaliana, among 10 members the Pi transport activity has been reported only for 3 members such as PHO1 (Hamburger et al., 2002; Stefanovic et al., 2007, 2011; Arpat et al., 2012), PHO1;H1 (Stefanovic et al., 2007), and PHO1;H3 (Khan et al., 2014). Similarly, in rice, only OsPHO1;2 seems to mediate the Pi transport effect that is comparable to PHO1 of A. thaliana (Secco et al., 2010). Further, four genes were identified in maize (Z. mays) similar to AtPHO1 and were designated as ZmPHO1;1, 1;2a, 1;2b, and 1;3 (Salazar-Vidal et al., 2016). Recently, as many as 69 SPX domain
containing genes including those similar to AtPHO1 have been identified, and expression analysis was characterized in rapeseed (Brassica napus) (Du et al., 2017).

6.3.3 Transcription factors Several TFs have been found to regulate the low Pi stress responses in plants (Fig. 6.4). Their role in maintaining Pi homeostasis has been well characterized during the last decade (Table 6.2). These TFs play a central role in regulating the low Pi stressresponsive genes (Gu et al., 2016). The key TF functioning to control the low Pi stressresponsive genes is PHOSPHATE STARVATION RESPONSE1 (PHR1) (Guo et al., 2015). PHR1 belongs to the MYB-CC family TFs, and it regulates the expression of low Pi stress-responsive genes by binding to the palindromic sequences (GNATATNC) called P1BS (PHR1-binding sequence) found in the promoters of Pi stress-responsive genes (Bustos et al., 2010). Apart from PHR1, several other TFs, such as MYB62, ZAT6, WRKY6, WRKY75, and PTF, have also been found to regulate the low Pi stress signaling in plants (Jain et al., 2012). PHT1s and several other low Pi stress-responsive genes seem to possess P1BS sequence in their promoter region. This P1Bs is bound by MYB TFs like PHR1/PHL1 in A. thaliana and PHR1 homologs in several other plants (Bustos et al., 2010; Guo et al., 2015). PHR1-P1BS component is the key regulator of low Pi stress signaling and transcriptionally activates many Pi stress-responsive genes in plants (Gu et al., 2016). Apart from PHR1s, other TFs are also found to be involved in low Pi stressresponsive signaling (Chen and Schmidt, 2015). In A. thaliana, AtMYB2 controls the expression of miR399 by binding to the MBS motif (consensus sequence TAACTG)

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FIGURE 6.4

Transcriptional and posttranscriptional regulation of genes involved in low Pi stress responses. Major TFs involved in the induction of key genes under low Pi stress condition are depicted. PHR1 is the key TF involved in the transcriptional activation of key genes like PHT1s under low Pi stress condition. Other members, such as WRKYs and MYB, also bind to the promoter of low Pi stress-responsive genes and activate the transcription under low Pi stress condition. miRNAs downregulate the genes by binding to the mRNA of key genes under low Pi stress condition. MiR399 is involved in the inhibition of PHO2 which mediates the degradation of PHT1s and PHO1 through ubiquitin-mediated endocytosis in vacuoles. MiR827 represses the transcript of NITROGEN LIMITATION ADAPTATION (NLA) which is also involved in PHT1 degradation. All these processes upregulate the low Pi stress-responsive genes and improves the Pi uptake under low Pi stress conditions. miRNAs, microRNAs; Pi, inorganic phosphate; TFs, transcription factors.

found in the promoter of miR399 (Baek et al., 2013). The PHT1s induced by AMF seem to possess the AMF-specific cis-element mycorrhiza TF-binding sequence (MYCS). Both MYCS and P1BS cause these PHT1 genes as AMF-specific in solanaceous plants (Ceasar et al., 2014; Chen et al., 2011). Another study confirmed that only MYCS (four tandem copies) alone is sufficient to induce the PHT1 expression with AMF colonization with L. japonicas (Lota et al., 2013). The presence of tandem signals for low Pi stress response and AMF induction reveal that low Pi stress and AMF symbiosis might share an overlapping and conserved signaling. WRKYs are other class of TFs involved in low Pi stress responses in plants. These TFs regulate the low Pi stress-responsive genes by binding to the W-box motifs in promoter of these genes. In A. thaliana, WRKY75 and 45 are upregulated by low Pi stress and had a positive effect on AtPHT1;1 gene (Devaiah et al., 2007a; Su et al., 2015). But WRKY6 and 42 TFs regulate the expression of PHO1 (Su et al., 2015). The WRKY42 TF was bound to the PHO1 promoter under high Pi condition, but binding was abolished under low Pi-stress condition, and this activated the PHO1 expression (Su et al., 2015; Chen et al., 2009). The TFs reported to regulate the low Pi stress responses are presented in Table 6.2.

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TABLE 6.2 Key transcription factors (TFs) and their role identified in the regulation of low Pi stress responses. Name of the TF

Type

Plant name

Function

Reference

AtPHR1

1R-type MYB-CC

Arabidopsis thaliana

Upregulation of PHT1s

Guo et al. (2015)

OsPHR2

1R-type MYB-CC

Rice

Upregulation of PHT1s

Liu et al. (2010) and Zhou et al. (2008)

PvPHR1

1R-type MYB-CC

Common bean

Upregulation of PHT1s

Valdes-Lopez et al. (2008)

TaPHR1

Wheat

Upregulation of PHT1s

Wang et al. (2013)

AtBHLH32

1R-type MYB-CC bHLH

A. thaliana

Downregulation of PEPCK

Chen et al. (2007b)

ZmPTF1

bHLH type Maize

Upregulation of PHT1s, FBP, and SPS

Li et al. (2011)

OsPTF1

bHLH type Rice

Upregulation of nutrient transport genes

Yi et al. (2005)

AtMYB2

R2R3-type MYB TF R2R3 MYB TF

A. thaliana

Upregulation of miR399f and LPSI

Baek et al. (2013)

Rice

Upregulation of PHT1s, OsmiR399a, and OsmiR399j

Dai et al. (2012)

Rice

Upregulation of PHT1s

Yang et al. (2014)

AtWRKY6

R2R3 MYB TF WRKY

A. thaliana

Downregulation of PHO1

Chen et al. (2009)

AtWRKY42

WRKY

A. thaliana

Upregulation of PHT1s and downregulation of PHO1

Su et al. (2015)

AtWRKY45

WRKY

A. thaliana

Upregulation of PHT1s

Wang et al. (2014a)

AtWRKY75

WRKY

A. thaliana

Upregulation of PHT1s

Devaiah et al. (2007a)

AtZAT6

Downregulation of PHT1s

Devaiah et al. (2007b)

OsARF12

Cys-2-His-2 A. thaliana Zinc finger TF ARF TF Rice

Upregulation of PHT1s and downregulation of SPX-MFS1

Wang et al. (2014b)

OsARF16

ARF TF

Downregulation of PHT1s

Shen et al. (2013)

OsMYB2P-1 OsMYB4P

Rice

Name of the specific TF, type, host plant, and function with reference are indicated for each TF. FBP, Fructose-1,6-bisphosphatase; LPSI, low phosphate stress induced; PEPCK, phosphoenolpyruvate carboxylase kinase; PHT1, Phosphate Transporter1; SPS, sucrose phosphate synthase1.

6.3.4 MicroRNAs miRNAs are involved in several important regulatory functions of plant growth, development, and low nutrient stress responses including low Pi stress signaling (Wu, 2013). Several miRNAs were also found to mediate the nutrient signaling between cells, tissues, and organs (Nguyen et al., 2015). In plants, about 21-nt-long RNAs were processed from

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stem-loop regions of lengthy primary transcripts and form silencing complexes, which direct the cleavage of complementary miRNAs (Jones-Rhoades et al., 2006). Therefore miRNAs regulate the genes by targeting their mRNAs by binding to nearly complementary sequences and function as posttranscriptional negative regulators (Fig. 6.4). In recent studies, several miRNAs have been found to regulate the low Pi stress-responsive gene expression in many plants (reviewed in Paul et al., 2015). The first miRNA to be identified in response to low Pi starvation is miRNA399 in A. thaliana, which is also found to be involved in shoot-to-root signaling during low Pi stress (Pant et al., 2008; Chiou, 2007). Low Pi starvation transmits signals to shoots and elicits the synthesis of miRNA399 which binds at 50 untranslated region (UTR), 200
400 bp upstream of the PHOSPHATE OVER ACCUMULATOR2 (PHO2) transcript. This binding induces cleavage of PHO2 mRNA (Pant et al., 2008). This effect helps to accumulate Pi in shoots during low Pi-stress conditions since degradation of PHO2 helps to improve the Pi uptake and translocation. PHO2 is an E-2 ubiquitin conjugating enzyme and negatively regulates the transporters such as PHT1s under high Pi conditions. It has been proved that pho2 mutants exhibit Pi toxicity in shoots due to overaccumulation of Pi in A. thaliana (Aung et al., 2006). The following studies also proved that miRNA399 was overexpressed with downregulation of PHO2 under low Pi-stress conditions (Chiou et al., 2006; Kuo and Chiou, 2011). Further, overexpression of miRNA399 improved Pi transport to shoots under high Pi that leads to Pi toxicity (Aung et al., 2006). In a recent study, it has been demonstrated that miRNA399 also had the same effect of transcriptional repression of PHO2 in maize under low Pi-stress condition (Du et al., 2018). The miRNA399 has been overexpressed by low Pi stress and transgenic plants overexpressing this miRNA translocated more Pi into the shoots. Further, a novel low Pi stress-responsive long-noncoding RNA1 (PILNCR1) was identified from RNA libraries. It has been demonstrated that PILNCR1 inhibits miRNA399-guided cleavage of maize ZmPHO2, which confirmed the interaction between PILNCR1 and miRNA399 for Pi-stress tolerance in maize (Du et al., 2018). Apart from miRNA399, other miRNAs were also involved in the regulation of low Pi stress responses in plants. miRNA827 also improves the shoot Pi content by targeting the 50 -UTR of NITROGEN LIMITATION ADAPTATION (NLA) mRNA (Kant et al., 2011). Under low N levels, the nla mutant accumulates excessive Pi and plays an important role in the regulation of Pi levels. Similarly, miRNA827-overexpressing A. thaliana plants had same effect, and it regulates PHT1 expression (Kant et al., 2011). Similarly, miRNA827 of rice has been found to mediate the Pi accumulation in shoots (Wang et al., 2012). Two other miRNAs, such as miRNA778 and miRNA2111, were also found to be involved in the regulation of low Pi stress responses. The miRNA2111 was identified by bioinformatics analysis using a miRDeep algorithm (Pant et al., 2009). The miRNA2111 has been predicted to be induced by low Pi stress. According to a latter study, activity of miR2111 was opposite under low N stress compared to low Pi stress (Liang et al., 2012). Further, low Pi stress-responsive miRNAs with varied responses to Pi starvation were also reported in soybean (Zeng et al., 2010). Several miRNAs, such as miR319a, miR396a, miR398b, and miRNA1507a, have been found to be downregulated and miRNA159a has been upregulated by low Pi stress (Zeng et al., 2010). Apart from miRNAs, a group of nonprotein coding genes, such as INDUCED BY PHOSPHATE STARVATION1 and At4, are highly induced by low Pi stress (Franco-Zorrilla et al., 2007). These RNAs have motif sequences

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complementary to miR399s. This binding enables these RNAs to inhibit miR399s from cleaving the PHO2 transcripts, providing an additional layer of antagonistic regulation by fine-tuning the activity of miRNA399s (Franco-Zorrilla et al., 2007). Although the miRNAs have been mostly studied in model plants such as A. thaliana and rice, regulation of low Pi stress by miRNAs are yet to be studied in many other crop plants. Expanding the studies on miRNAs in other plants will also help to understand the roles of these and any novel miRNAs in low Pi-stress regulation.

6.4 Role of arbuscular mycorrhizae fungal in low phosphate stress tolerance AMF also plays key roles on enhanced uptake of Pi at root and soil interface, especially under low Pi stress. AMF colonization is a symbiotic association by which both partners (plant and fungus) are benefited through bidirectional nutrient transfer. The AMF helps for the enhanced uptake of nutrients, especially Pi; in return, AMF receives the photosynthetically fixed sugar from the plants. The AMF fungi under the phylum Glomeromycota are a group of endophytes, and these can form symbiosis with the roots of B80% plant species (Remy et al., 1994; Smith and Gianinazzi-Pearson, 1988). The AMF colonization significantly improves the nutrient uptake especially Pi uptake (Smith and Read, 2008). As P is a highly immobile element due to fixation by microbes and interaction with cations, a Pi-depletion zone rapidly occurs around plant roots. The AMF forms extraradical mycelium, which can be very extensive in the soil and increase prominently the Pi absorbing area of roots, especially beyond the Pi-depletion zone (Smith and Gianinazzi-Pearson, 1988). Plants colonized with AMF exhibit a separate Pi uptake pathway which is distinct from direct uptake by epidermis of root hairs. The AMF-mediated Pi uptake begins at the extraradical hyphae in the soil, translocated toward the roots, and released from the arbuscule into the periarbuscular space (Bucher, 2007; Smith et al., 2011). It is really interesting to note that AMF-specific PHT1 family Pi transporters are induced in plants to uptake the Pi across the plant’s periarbuscular membrane (Bucher, 2007). In fungi, two AMF-specific Pi transporters, such as GvPT form Glomus versiforme and GiPT from G. intraradices, were identified in fungal species from the Basidiomycota and Ascomycota, respectively (Harrison and Buuren, 1995; Maldonado-Mendoza et al., 2001). The GvPT and GiPT genes are found to be expressed predominantly in the extraradical fungal mycelium exposed to μM levels of Pi (Maldonado-Mendoza et al., 2001). The PHT1 family genes induced by AMF are very crucial for AMF-mediated Pi uptake. The AMF-specific PHT1 family gene was first identified in potato (Rausch et al., 2001). Following this, several AMF-specific PHT1 transporters are being identified and reported in several plants (Baker et al., 2015). Plants colonized by AMF seem to possess a few PHT1 transporters specific to AMF and are induced only during colonization by AMF (Table 6.3). Several mycorrhiza-inducible PHT1s were reported in the plants colonized with AMF (Xie et al., 2013). These include MtPHT1;4 in barrel medic (Harrison et al., 2002); OsPHT1;11 and OsPHT1;13 in rice (Paszkowski et al., 2002; Glassop et al., 2007); StPHT1;3, StPHT1;4, and StPHT1;5 in potato (Rausch et al., 2001; Nagy et al., 2005); GmPHT1;7, GmPHT1;10, and GmPHT1;11 in soybean (Tamura et al., 2012); AsPHT1;1 in Astragalus sinicus (Xie et al., 2013); ZmPHT1;6 in maize (Karasawa et al., 2012); SiPHT1;8 and SiPHT1;9 in foxtail millet (Ceasar et al., 2014);

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TABLE 6.3 Details on Phosphate Transporter1 (PHT1) genes expressed by arbuscular mycorrhizae fungi (AMF) colonization in plants. Plant species

AMF species used

Reference

AsPHT1;1, AsPHT1;3, AsPHT1;4

Chinese milkvetch

Gigaspora margarita and Glomus intraradices

Xie et al. (2013)

BdPHT1;3, BdPHT1;7, BdPHT1;12, BdPHT1;13

Purple false Glomus candidum brome

Hong et al. (2012)

CfPHT1;3, CfPHT1;4, CfPHT1;5

Red pepper G. intraradices

Chen et al. (2007a)

Name of the PHT1 gene

GmPHT1;11, GmPHT1;12, GmPHT1;13 Soybean

G. intraradices

Tamura et al. (2012)

HvPHT1;8 HvPHT1;11

Barley

G. intraradices, Glomus sp., WFVAM23, and Scutellospora calospora

Glassop et al. (2005) and Sisaphaithong et al. (2012)

LjPHT1;3 LjPHT1;4

Miyakogusa Glomus mosseae, G. intraradices

MtPHT1;1, MtPHT1;4

Barrel clover

Glomus versiforme

Harrison et al. (2002) and Javot et al. (2007)

OsPHT1;11, OsPHT1;13

Rice

G. intraradices

Paszkowski et al. (2002) and Guimil et al. (2005)

OsPHT1;11, OsPHT1;13

Rice

G. intraradices

Glassop et al. (2007)

PhPHT1;3, PhPHT1;4, PhPHT1;5

Petunia

G. intraradices

Wegmu¨ller et al. (2008)

PtaPHT1;4

Hardy orange

Glomus etunicatum, Glomus diaphanum, and G. versiforme

Shu et al. (2012)

PtPHT1;9, PtPHT1;10, PtPHT1;12

Black G. intraradices and G. mosseae cottonwood

SiPHT1;8, SiPHT1;9

Foxtail millet

G. mosseae

Ceasar et al. (2014)

SlPHT1;3, SlPHT1;4, SlPHT1;5

Tomato

Glomus margarita, Glomus caledonium, and G. intraradices

Nagy et al. (2005)

SmePHT1;3, SmePHT1;4, SmePHT1;5

Eggplant

G. intraradices

Chen et al. (2007a)

StPHT1;3, StPHT1;4, StPHT1;5

Potato

G. intraradices

Rausch et al. (2001) and Nagy et al. (2005)

TaPHT1;8, TaPHT1;10, TaPHT1;11, TaPHT1;12

Wheat

Glomus sp., WFVAM23, S. calospora, and G. intraradices

ZmPHT1;6

Maize

G. intraradices

Glassop et al. (2005) Sisaphaithong et al. (2012) Nagy et al. (2006)

ZmPHT1;2, ZmPHT1;4, ZmPHT1;6, ZmPHT1;7, ZmPHT1;9, and ZmPHT1;11

Maize

G. etunicatum

Liu et al. (2016a)

Maeda et al. (2006)

Loth-Pereda et al. (2011)

(Continued)

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TABLE 6.3 (Continued) Name of the PHT1 gene

Plant species

SbPHT1;9 and SbPHT1;10

AMF species used

Reference

Sorghum

Rhizophagus irregularis and Funeliformis mosseae

Walder et al. (2015)

LuPHT1;5 and LuPHT1;8

Flax

R. irregularis and F. mosseae

Walder et al. (2015)

ZmPHT1;9

Maize

G. etunicatum

Liu et al. (2018b)

VvPHT1;1 and VvPHT1;2

Grapes

F. mosseae

Valat et al. (2018)

EcPHT1;4

Finger millet

G. intraradices

Pudake et al. (2017)

The PHT1 genes expressed by AMF colonization are listed including the name of the AMF species used and name of the plant. AMF, Arbuscular mycorrhizae fungi.

and SlPHT1;4 and SlPHT1;5 in tomato (Chen et al., 2007a; Xu et al., 2007). Recently (Eleusine coracana) EcPHT1;4 has been found to be induced by AMF G. intraradices in finger millet (Pudake et al., 2017). So the AMF colonization also helps in maintaining low Pi stress responses in most of the crop plants and will help to overcome low Pi stress under natural field conditions by improving Pi uptake.

6.5 Biochemical responses to low phosphate stress 6.5.1 Hormones Several hormones have been proposed to modulate the RSA under low Pi stress, including arrest of primary root growth with the proliferation of lateral roots and root hairs. Changes in the levels of plant hormones, such as auxin and increased sensitivity to auxin, have been reported under low Pi-stress conditions (Lo´pez-Bucio et al., 2002, 2005; Pe´rezTorres et al., 2008). Under low Pi stress, pericycle cells increase the sensitivity to auxin, and this has been found to be important for lateral root induction (Lo´pez-Bucio et al., 2002; Pe´rez-Torres et al., 2008). Further, it was revealed that the expression of the A. thaliana auxin receptor TIR1 (discussed earlier) is higher under low Pi condition when compared to high Pi condition (Pe´rez-Torres et al., 2008). The knockdown of TIR1 inhibited the production of lateral roots under low Pi-stress condition. Differential accumulation of auxin has also been found to be important for the emergence of lateral roots (Nacry et al., 2005). More recently, Lynch group reported that auxin is also critical for the growth of root hair in A. thaliana under low Pi stress (Bhosale et al., 2018). They studied the effect using mutants involved in auxin synthesis (taa1) and transport (aux1), both these mutants abolished the low Pi stress related root hair response. Specific expression of AUX1 rescued the low Pi stress responses in aux1 mutants. Hence, transport of auxin from the root apex to differentiation zone aids in the auxin-dependent RSA changes, especially root hair responses under low Pi stress. So auxin plays a critical role in regulating the root adaptive

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responses under low Pi stress (Bhosale et al., 2018). Another plant hormone strigolactone is also involved in the regulation of root development (Waldie et al., 2014). It has been proved in rice that strigolactones altered the primary root growth in low Pi-stress condition (Sun et al., 2014).

6.5.2 Sugars Sugars play several important functions on regulation of low Pi stress, and plant Pi status is closely related to photosynthesis and carbon levels (Wissuwa et al., 2005). Like miRNAs, sugars are also involved in long-distance Pi signaling from shoot to root (reviewed in Lo´pez-Arredondo et al., 2014). Past studies on this field have proved that sucrose and other carbohydrates are involved in long-distance signaling of low Pi stress response and especially shoot-to-root transport of sugars through the phloem (Karthikeyan et al., 2007; Mu¨ller et al., 2005, 2007; Liu et al., 2005). Several studies in recent years have shed light on the regulation of the Pi by sugars, specifically on the role of sugars in physiological, biochemical, and molecular responses to low Pi stress (Hammond and White, 2008). In order to maintain the tightly controlled levels of Pi concentration, expression of PHT genes (viz., PHT2) have been found to be controlled by sucrose concentration (Lejay et al., 2003). Two other members of Pi transporters, PHT1;4 and 3;1, were also found to be regulated by sucrose supply in A. thaliana (Lejay et al., 2008). Pi deficiency elevated the levels of sucrose in shoot and root tissues in common bean (Ciereszko and Barbachowska, 2000; Ciereszko et al., 1996) and soybean (Fredeen et al., 1989). As discussed earlier, induction of root hair under low Pi stress was also seen under the external supply of sucrose (Jain et al., 2007). Sugars are also proved to elevate the expression levels of many low Pi stress-responsive genes (Karthikeyan et al., 2007; Liu et al., 2005; Hammond and White, 2011). In white lupin the low Pi stress-responsive genes LaPHT1;1 and acid phosphatase (LaSAP1) were induced by exogenous supply of sucrose even in normal Pi conditions. Interestingly, expressions of these genes are blocked in roots under low Pi conditions (Liu et al., 2005). PHOSPHATE3 (PHO3) is involved in sucrose loading into phloem, and the expression of low Pi stress-responsive genes in root is impaired in the A. thaliana pho3 mutants (Zakhleniuk et al., 2001). Sucrose levels were elevated in both shoot and root of the plants overexpressing SUCROSE TRANSPORTER 2 (SUC2) involved in sucrose transport, in the hypersensitive to phosphate starvation 1 (hps1) mutants, and this leads to the induction of several low Pi starvation responsive genes under normal supply of Pi (Lei et al., 2011; Lloyd and Zakhleniuk, 2004). These studies have further substantiated the involvement of sugars in signaling for the regulation of low Pi stress responses in plants.

6.5.3 Inositol pyrophosphates Involvement of inositol pyrophosphates (PP-InsPs) to regulate the low Pi stress response has recently been investigated using a combined genetic, structural, and biochemical approach (Wild et al., 2016). As discussed earlier, SPX-containing proteins play key role in the regulation of low Pi stress response. The interaction of PP-InsPs with SPX

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domains of proteins involved in low Pi stress response has been reported in plant, fungal, and human SPX proteins (Jung et al., 2018). PP-InsPs have proved to be the ligands for the SPX domain, and PP-InsPs complex interacts with SPX domain with nM to μM affinity. The inositol ring of the PP-InsPs complex is completely phosphorylated with extra PP groups in one or more positions (Shears, 2015). Previously, it was thought that Pi itself could interact with SPX domain and regulate the expression of low Pi stress responsible genes. Earlier works on SPX domains proved that SPX domain can interact with the PHR1 TFs in A. thaliana and rice (PHR2 in rice) (Puga et al., 2014; Lv et al., 2014; Wang et al., 2014d). Both PHR1 and PHR2 induce the transcription of low Pi stress-responsive genes under deplete condition by interacting with SPX proteins (Lv et al., 2014). Binding of PHR1/2 to its target promoters is prevented by the SPX-PHR1/2 complex under sufficient Pi conditions. But, at low Pi stress, PHR1/2 is not bound to SPX, and the free PHT1/2 can induce the expression of low Pi stress-responsive genes. In a recent study involving structural and biochemical characterization of SPX domain, it has been demonstrated that highaffinity (7
50 μM) interaction of SPX4 and PHR2 in rice is promoted by PP-InsPs, confirming that PHR1/2’s activity is regulated by PP-InsPs through SPX proteins (Wild et al., 2016). These interactions induce the high-level expression of low Pi stress-responsive genes to improve the Pi uptake under deplete Pi conditions.

6.5.4 Lipids Changes in the composition of lipids are a major biochemical change reported under low Pi-stress condition in plants. Especially, recent studies shed more light on molecular events involved in the alteration of lipid composition induced by low Pi starvation (Nakamura, 2013). Under low Pi stress, Pi is released from plants by the cleavage of Pi from organic molecules that contain Pi such as phospholipids and Pi-esters. In plants, B15%
30% of Pi is found in the form of phospholipids (Poirier et al., 1991). The phospholipids are converted into other forms of lipids, namely monogalactosyldiacylglycerol, digalactosyldiacylglycerol (DGDG), and sulfooquinovosyldiacylglycerol (SQDG) under low Pistress condition (Shimojima and Ohta, 2011). The most important changes occurred during low Pi starvations are the degradation of phospholipids to release Pi, and the phospholipids will be substituted by glycolipids. Particularly, phosphatidylglycerol was replaced by SQDG in the chloroplast under low Pi-stress condition (Essigmann et al., 1998). DGDG is an important lipid for lipid remodeling under low Pi stress, and DGDG levels were increased about twofold in A. thaliana leaves with parallel decrease of phospholipids under low Pi conditions (Kelly et al., 2003; Li et al., 2006). Even the plasma membrane has also been found to be altered with the replacement of phospholipids by glycolipids under low Pi-stress condition in oat plants (Andersson et al., 2003).

6.5.5 Exudation of organic acids from roots Production and release of organic acids (OAs) from roots are an important response of plants under low Pi-stress conditions to increase the availability of Pi. These are helpful to solubilize Pi fixed with cations, especially at topsoil layers (Baker et al., 2015). The major

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6. Regulation of low phosphate stress in plants

OAs released by roots include citrate, malate, and oxalate, which help to release the Pi bound to Al31, Fe31, and Ca21 by chelating the metals (Ryan et al., 2001). Among the OAs, citrate and oxalate were found to show superior effect on releasing the Pi when compared to malate, lactate, and succinate (Ryan et al., 2001). Each plant seems to release different OA due to low Pi starvation. In pigeon pea the exudation of piscidate from roots was involved to release Pi fixed as Fe
P (Ae et al., 1990). However, citrate secreted from proteoid roots was involved in the release of Pi fixed as Fe
P in white lupin (Gardner et al., 1983). In sugar beets, citramalate and salicylate were the major OAs released under low Pi stress, and both these OAs helped in the release of Pi from cations (Khorassani et al., 2011). Recent studies also proved that the efficient genotypes and species of low Pistress tolerance produced more amount of OAs than inefficient genotypes in several plants including A. thaliana (Narang et al., 2000), maize (Hinsinger, 2001), barley (Gahoonia et al., 2000), and rapeseed (B. napus) (Zhang et al., 2011; Zhou et al., 2012). Similarly, cabbage (Brassica oleracea) was superior to carrot (Daucus carota) and potato (Solanum tuberosum) in secretion of citrate and had higher low Pi-stress tolerance, whereas potato and carrot displayed inferior response for such mechanism (Dechassa and Schenk, 2004). The OAs were mainly released at the root tip, but it was also released from the proteoid roots in some plants such as white lupin under low Pi stress. This action by the proteoid roots not only helps in improved topsoil scavenging of Pi but also secretes mM concentration of citrate and malate at rhizosphere for additional release of Pi under low Pi stress (Jones et al., 1996; Vance et al., 2003; Lambers et al., 2013). In addition, the intracellular concentration of OAs is not equal to the levels released around the rhizosphere in all plants. For example, wheat and tomato plants release very minimal amounts of OAs, although they possess increased concentration of OAs under low Pi-stress conditions indicating the importance of specific transporters for these OAs (Lo´pezArredondo et al., 2014). Transporters mediate the release of malate and citrate has been identified. Malate has been found to be transported through a plasma membrane
bound aluminum-activated malate transporter (Hoekenga et al., 2006), while citrate has been transported by the multidrug and toxic compound extrusion (MATE) family transporters (Sasaki et al., 2004). The MATE transporters are also found to show tolerance to aluminum toxicity in A. thaliana and sorghum (Liu et al., 2009; Magalhaes et al., 2007). However, further functions of these genes in many other plants are yet to be validated. Exploitation of OA exudation trait has been considered as one of the important breeding objectives to improve the low Pi-stress tolerance and improve the PUE in crop plants.

6.5.6 Release of acid phosphatases Plants secrete acid phosphatases (APases) into the apoplastic space for the digestion and release of Pi from organic sources under low Pi-stress conditions. It was first demonstrated in A. thaliana using phosphatase under-producer (pup) mutants (Tomscha et al., 2004). The APases activity around the root was decreased by .16% in pup mutants. Following this, a specific enzyme, acid phosphatase10 (AtPAP10) released under Pi stress response in A. thaliana was reported using genetic and molecular approaches (Wang et al., 2011b). Similarly, a purple APases linked to the low Pi stress response has been identified and

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characterized in the roots of common bean (P. vulgaris). Furthermore, expression of PvPAP3 was higher in a P-efficient genotype (G19833) when compared to P-inefficient genotype (DOR364) (Liang et al., 2010). In soybean, overexpression of A. thaliana purple APase gene (AtPAP15) increased the APase activity by 1.5-fold and significantly improved the Pi uptake (Wang et al., 2009). Several other reports also confirmed that overexpression of APases through transgenic modification improved the low Pi stress tolerance by enhanced release of Pi from organic sources (Lo´pez-Arredondo et al., 2014).

6.6 Conclusion and future prospects The natural rock phosphate reserves are very finite and are depleting at a rapid pace with a prediction of getting extinguished in 100 years or soon. It is very difficult to produce crops without the supply of synthetic P fertilizers. The mechanisms involved in low Pi stress response in plants have been well documented in the past decade. All plants studied so far seem to change their RSA in response to low P stress for increased topsoil foraging from soil solution. The genes, TFs, miRNAs, sugars, and hormones involved in the regulation of low Pi stress tolerance have been well documented. Among these, the PHT1 genes encoding transporters for the uptake of Pi from soil are the primary targets for improved uptake of Pi. Several other Pi transporters involved in transport to shoots and intracellular organelles were characterized. TFs, such as PHR1 that are involved in the regulation of low Pi stress-response genes, have been studied. Several plants are also known to interact with AMF to improve the Pi uptake under low Pi stress conditions with the expression of AMF-specific PHT1 genes. Several hormones, sugars, and OAs were also modulated under low Pi-stress conditions. Most of these studies have been performed in model plant A. thaliana. Only a few studies have been attempted in crop plants. Further studies on characterization of these responses in other crop plants will help to improve the PUE especially in orphan crops such as millets which are cultivated in less-developed countries. This will help to improve the sustainable agriculture and ensure food security in future.

References Ae, N., Arihara, J., Okada, K., Yoshihara, T., Johansen, C., 1990. Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent. Science 248 (4954), 477
480. Ai, P., Sun, S., Zhao, J., Fan, X., Xin, W., Guo, Q., et al., 2009. Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant J. 57 (5), 798
809. Andersson, M.X., Stridh, M.H., Larsson, K.E., Liljenberg, C., Sandelius, A.S., 2003. Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett. 537 (1), 128
132. Arpat, A.B., Magliano, P., Wege, S., Rouached, H., Stefanovic, A., Poirier, Y., 2012. Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. Plant J. 71 (3), 479
491. Aung, K., Lin, S.I., Wu, C.C., Huang, Y.T., Su, C.L., Chiou, T.J., 2006. pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 141 (3), 1000
1011. Ayadi, A., David, P., Arrighi, J.F., Chiarenza, S., Thibaud, M.C., Nussaume, L., et al., 2015. Reducing the genetic redundancy of Arabidopsis Phosphate transporter1 transporters to study phosphate uptake and signaling. Plant Physiol. 167 (4), 1511
1526.

Plant Life under Changing Environment

146

6. Regulation of low phosphate stress in plants

Baek, D., Kim, M.C., Chun, H.J., Kang, S., Park, H.C., Shin, G., et al., 2013. Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol. 161 (1), 362
373. Baker, A., Ceasar, S.A., Palmer, A.J., Paterson, J.B., Qi, W., Muench, S.P., et al., 2015. Replace, reuse, recycle: improving the sustainable use of phosphorus by plants. J. Exp. Bot. 66 (12), 3523
3540. Bhosale, R., Giri, J., Pandey, B.K., Giehl, R.F.H., Hartmann, A., Traini, R., et al., 2018. A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat. Commun. 9 (1), 1409
1417. Borch, K., Bouma, T.J., Lynch, J.P., Brown, K.M., 1999. Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ. 22 (4), 425
431. Bucher, M., 2007. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol. 173 (1), 11
26. Bucher, M., Fabianska, I., 2016. Long-sought vacuolar phosphate transporters identified. Trends Plant Sci. 21 (6), 463
466. Bustos, R., Castrillo, G., Linhares, F., Puga, M.I., Rubio, V., Perez-Perez, J., et al., 2010. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 6 (9), e1001102. Cao, Y., Sun, D., Chen, J.X., Mei, H., Ai, H., Xu, G., et al., 2018. Phosphate transporter PvPht1;2 enhances phosphorus accumulation and plant growth without impacting arsenic uptake in plants. Environ. Sci. Technol. 52 (7), 3975
3981. Carswell, C., Grant, B.R., Theodorou, M.E., Harris, J., Niere, J.O., Plaxton, W.C., 1996. The fungicide phosphonate disrupts the phosphate-starvation response in Brassica nigra seedlings. Plant Physiol. 110 (1), 105
110. Ceasar, S.A., 2018. Feeding world population amidst depleting phosphate reserves: the role of biotechnological interventions. Open Biotechnol. J. 12, 51
55. Ceasar, S.A., Hodge, A., Baker, A., Baldwin, S.A., 2014. Phosphate concentration and arbuscular mycorrhizal colonisation influence the growth, yield and expression of twelve PHT1 family phosphate transporters in foxtail millet (Setaria italica). PLoS One 9 (9), e108459. Ceasar, S.A., Baker, A., Muench, S.P., Ignacimuthu, S., Baldwin, S.A., 2016. The conservation of phosphatebinding residues among PHT1 transporters suggests that distinct transport affinities are unlikely to result from differences in the phosphate-binding site. Biochem. Soc. Trans. 44 (5), 1541
1548. Ceasar, S.A., Baker, A., Ignacimuthu, S., 2017. Functional characterization of the PHT1 family transporters of foxtail millet with development of a novel Agrobacterium-mediated transformation procedure. Sci. Rep. 7, e14064. Chao, M., Zhang, Z., Song, H., Li, C., Zhang, X., Hu, G., et al., 2017. Genome-wide identification and expression analysis of Pht1 family genes in cotton (Gossypium hirsutum L.). Cotton Sci. 29 (1), 59
69. Chen, C.Y., Schmidt, W., 2015. The paralogous R3 MYB proteins caprice, triptychon and enhancer of try and CPC1 play pleiotropic and partly non-redundant roles in the phosphate starvation response of Arabidopsis roots. J. Exp. Bot. 66 (15), 4821
4834. Chen, A., Hu, J., Sun, S., Xu, G., 2007a. Conservation and divergence of both phosphate- and mycorrhizaregulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol. 173 (4), 817
831. Chen, Z.H., Nimmo, G.A., Jenkins, G.I., Nimmo, H.G., 2007b. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem. J. 405 (1), 191
198. Chen, Y.F., Li, L.Q., Xu, Q., Kong, Y.H., Wang, H., Wu, W.H., 2009. The WRKY6 transcription factor modulates Phosphate 1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21 (11), 3554
3566. Chen, A., Gu, M., Sun, S., Zhu, L., Hong, S., Xu, G., 2011. Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytol 189 (4), 1157
1169. Chen, A., Chen, X., Wang, H., Liao, D., Gu, M., Qu, H., et al., 2014. Genome-wide investigation and expression analysis suggest diverse roles and genetic redundancy of Pht1 family genes in response to Pi deficiency in tomato. BMC Plant Biol. 14 (1), 61
75. Chen, J., Wang, Y., Wang, F., Yang, J., Gao, M., Li, C., et al., 2015. The rice CK2 kinase regulates trafficking of phosphate transporters in response to phosphate levels. Plant Cell 27 (3), 711
723. Chiou, T.J., 2007. The role of microRNAs in sensing nutrient stress. Plant Cell Environ. 30 (3), 323
332. Chiou, T.J., Aung, K., Lin, S.I., Wu, C.C., Chiang, S.F., Su, C.I., 2006. Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18 (2), 412
421.

Plant Life under Changing Environment

References

147

Ciereszko, I., Barbachowska, A., 2000. Sucrose metabolism in leaves and roots of bean (Phaseolus vulgaris L.) during phosphate deficiency. J. Plant Physiol. 156 (5), 640
644. Ciereszko, I., Gniazdowska, A., Mikulska, M., Rychter, A.M., 1996. Assimilate translocation in bean plants (Phaseolus vulgaris L.) during phosphate deficiency. J. Plant Physiol. 149 (3), 343
348. Cordell, D., Drangert, J.O., White, S., 2009. The story of phosphorus: global food security and food for thought. Global Environ. Change 19 (2), 292
305. Cubero, B., Nakagawa, Y., Jiang, X.Y., Miura, K.J., Li, F., Raghothama, K.G., et al., 2009. The phosphate transporter PHT4;6 is a determinant of salt tolerance that is localized to the Golgi apparatus of Arabidopsis. Mol. Plant 2 (3), 535
552. Dai, X., Wang, Y., Yang, A., Zhang, W.H., 2012. OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiol. 159 (1), 169
183. Daram, P., Brunner, S., Rausch, C., Steiner, C., Amrhein, N., Bucher, M., 1999. Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. Plant Cell 11 (11), 2153
2166. Datta, S., Prescott, H., Dolan, L., 2015. Intensity of a pulse of RSL4 transcription factor synthesis determines Arabidopsis root hair cell size. Nat. Plants 1 (10), 15138
15144. Dechassa, N., Schenk, M.K., 2004. Exudation of organic anions by roots of cabbage, carrot, and potato as influenced by environmental factors and plant age. J. Plant Nut. Soil Sci. 167 (5), 623
629. Devaiah, B.N., Karthikeyan, A.S., Raghothama, K.G., 2007a. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 143 (4), 1789
1801. Devaiah, B.N., Nagarajan, V.K., Raghothama, K.G., 2007b. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol. 145 (1), 147
159. Dinkelaker, B., Hengeler, C., Marschner, H., 1995. Distribution and function of proteoid roots and other root clusters. Bot. Acta 108 (3), 183
200. DiTusa, S.F., Fontenot, E.B., Wallace, R.W., Silvers, M.A., Steele, T.N., Elnagar, A.H., et al., 2016. A member of the Phosphate transporter 1 (Pht1) family from the arsenic-hyperaccumulating fern Pteris vittata is a high-affinity arsenate transporter. New Phytol 209 (2), 762
772. Du, H., Yang, C., Ding, G., Shi, L., Xu, F., 2017. Genome-wide identification and characterization of SPX domaincontaining members and their responses to phosphate deficiency in Brassica napus. Front. Plant Sci. 8 (35), e103389. Du, Q., Wang, K., Zou, C., Xu, C., Li, W.X., 2018. The PILNCR1-miR399 regulatory module is important for low phosphate tolerance in maize. Plant Physiol. 177 (4), 1743
1753. Eswar, N., Webb, B., Marti-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M.-Y., et al., 2001. Comparative protein structure modeling using MODELLER. Current Protocols in Protein Science. John Wiley & Sons, Inc. Essigmann, B., Guler, S., Narang, R.A., Linke, D., Benning, C., 1998. Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 95 (4), 1950
1955. Fan, C., Wang, X., Hu, R., Wang, Y., Xiao, C., Jiang, Y., et al., 2013. The pattern of phosphate transporter 1 genes evolutionary divergence in Glycine max L. BMC Plant Biol. 13 (1), 48
63. Franco-Zorrilla, J.M., Valli, A., Todesco, M., Mateos, I., Puga, M.I., Rubio-Somoza, I., et al., 2007. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39 (8), 1033
1048. Fredeen, A.L., Rao, I.M., Terry, N., 1989. Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiol. 89 (1), 225
230. Gahoonia, T.S., Asmar, F., Giese, H., Gissel-Nielsen, G., Erik Nielsen, N., 2000. Root-released organic acids and phosphorus uptake of two barley cultivars in laboratory and field experiments. Eur. J. Agron. 12 (3), 281
289. Gamuyao, R., Chin, J.H., Pariasca-Tanaka, J., Pesaresi, P., Catausan, S., Dalid, C., et al., 2012. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488 (7412), 535
541. Gardner, W.K., Barber, D.A., Parbery, D.G., 1983. The acquisition of phosphorus by Lupinus albus L. Plant Soil 70 (1), 107
124. Glassop, D., Smith, S.E., Smith, F.W., 2005. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222 (4), 688
698. Glassop, D., Godwin, R.M., Smith, S.E., Smith, F.W., 2007. Rice phosphate transporters associated with phosphate uptake in rice roots colonised with arbuscular mycorrhizal fungi. Can. J. Bot. 85 (7), 644
651.

Plant Life under Changing Environment

148

6. Regulation of low phosphate stress in plants

Gonza´lez-Mendoza, V., Zurita-Silva, A., Sa´nchez-Caldero´n, L., Sa´nchez-Sandoval, M.E., Oropeza-Aburto, A., Gutie´rrez-Alanı´s, D., et al., 2013. APSR1, a novel gene required for meristem maintenance, is negatively regulated by low phosphate availability. Plant Sci. 2 (12), 205
206. Gruber, B.D., Giehl, R.F.H., Friedel, S., von Wire´n, N., 2013. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol. 163 (1), 161
179. Gru¨n, A., Buchner, P., Broadley, M., Hawkesford, M., 2018. Identification and expression profiling of Pht1 phosphate transporters in wheat in controlled environments and in the field. Plant Biol. 20 (2), 374
389. Gu, M., Chen, A., Sun, S., Xu, G., 2016. Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: what is missing? Mol. Plant. 9 (3), 396
416. Guimil, S., Chang, H.S., Zhu, T., Sesma, A., Osbourn, A., Roux, C., et al., 2005. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Natl. Acad. Sci 102 (22), 8066
8070. Guo, B., Jin, Y., Wussler, C., Blancaflor, E.B., Motes, C.M., Versaw, W.K., 2008. Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol. 177 (4), 889
898. Guo, W., Zhao, J., Li, X., Qin, L., Yan, X., Liao, H., 2011. A soybean beta-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J. 66 (3), 541
552. Guo, C., Guo, L., Li, X., Gu, J., Zhao, M., Duan, W., et al., 2014. TaPT2, a high-affinity phosphate transporter gene in wheat (Triticum aestivum L.), is crucial in plant Pi uptake under phosphorus deprivation. Acta Physiol. Plant. 36 (6), 1373
1384. Guo, M., Ruan, W., Li, C., Huang, F., Zeng, M., Liu, Y., et al., 2015. Integrative comparison of the role of the Phosphate Response1 subfamily in phosphate signaling and homeostasis in rice. Plant Physiol. 168 (4), 1762
1776. Ham, B.K., Chen, J., Yan, Y., Lucas, W.J., 2018. Insights into plant phosphate sensing and signaling. Curr. Opin. Biotechnol. 49, 1
9. Hamburger, D., Rezzonico, E., MacDonald-Comber Pete´tot, J., Somerville, C., Poirier, Y., 2002. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14 (4), 889
902. Hammond, J.P., White, P.J., 2008. Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J. Exp. Bot. 59 (1), 93
109. Hammond, J.P., White, P.J., 2011. Sugar signaling in root responses to low phosphorus availability. Plant Physiol. 156 (3), 1033
1040. Harrison, M.J., Buuren, M.L.V., 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378 (6557), 626
629. Harrison, M.J., Dewbre, G.R., Liu, J.Y., 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14 (10), 2413
2429. Hinsinger, P., 2001. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237 (2), 173
195. Hoekenga, O.A., Maron, L.G., Pin˜eros, M.A., Canc¸ado, G.M.A., Shaff, J., Kobayashi, Y., et al., 2006. AtALMT1 which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103 (25), 9738
9743. Hong, J.J., Park, Y.S., Bravo, A., Bhattarai, K.K., Daniels, D.A., Harrison, M.J., 2012. Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236, 851
865. Huang, C.Y., Shirley, N., Genc, Y., Shi, B., Langridge, P., 2011. Phosphate utilization efficiency correlates with expression of low-affinity phosphate transporters and non-coding RNA, IPS1 in barley. Plant Physiol. 156 (111), 1217
1229. Irigoyen, S., Karlsson, P.M., Kuruvilla, J., Spetea, C., Versaw, W.K., 2011. The sink-specific plastidic phosphate transporter PHT4;2 influences starch accumulation and leaf size in Arabidopsis. Plant Physiol. 157 (4), 1765
1777. Jain, A., Poling, M.D., Karthikeyan, A.S., Blakeslee, J.J., Peer, W.A., Titapiwatanakun, B., et al., 2007. Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol. 144 (1), 232
247. Jain, A., Nagarajan, V.K., Raghothama, K.G., 2012. Transcriptional regulation of phosphate acquisition by higher plants. Cellular and molecular life sciences. CMLS 69 (19), 3207
3224. Javot, H., Penmetsa, R.V., Terzaghi, N., Cook, D.R., Harrison, M.J., 2007. A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci 104 (5), 1720
1725. Jia, H., Ren, H., Gu, M., Zhao, J., Sun, S., Chen, J., et al., 2011. The Phosphate transporter gene, OsPht1;8, is involved in phosphate homeostasis in rice. Plant Physiol. 156 (3), 1164
1175.

Plant Life under Changing Environment

References

149

Jia, F., Wan, X., Zhu, W., Sun, D., Zheng, C., Liu, P., et al., 2015. Overexpression of mitochondrial phosphate transporter 3 severely hampers plant development through regulating mitochondrial function in Arabidopsis. PLoS One 10 (6), e0129717. Jin, J., Tang, C., Armstrong, R., Sale, P., 2012. Phosphorus supply enhances the response of legumes to elevated CO2 (FACE) in a phosphorus-deficient vertisol. Plant Soil 358 (1), 91
104. Jones, D.L., Darah, P.R., Kochian, L.V., 1996. Critical evaluation of organic acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant Soil 180 (1), 57
66. Jones-Rhoades, M.W., Bartel, D.P., Bartel, B., 2006. MicroRNAS and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19
53. Julia, C.C., Rose, T.J., Pariasca-Tanaka, J., Jeong, K., Masuda, T., Wissuwa, M., 2018. Phosphorus uptake commences at the earliest stages of seedling development in rice (Oryza sativa L.). J. Exp. Bot. Available from: https://doi.org/10.1093/jxb/ery267. Jung, J.Y., Ried, M.K., Hothorn, M., Poirier, Y., 2018. Control of plant phosphate homeostasis by inositol pyrophosphates and the SPX domain. Curr. Opin. Biotechnol. 49, 156
162. Kant, S., Peng, M., Rothstein, S.J., 2011. Genetic regulation by NLA and MicroRNA827 for maintaining nitratedependent phosphate homeostasis in Arabidopsis. PLoS Genet. 7 (3), e1002021. Karandashov, V., Nagy, R., Wegmuller, S., Amrhein, N., Bucher, M., 2004. Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 101 (16), 6285
6290. Karasawa, T., Hodge, A., Fitter, A.H., 2012. Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil. Plant Cell Environ. 35 (4), 819
828. Karthikeyan, A.S., Varadarajan, D.K., Jain, A., Held, M.A., Carpita, N.C., Raghothama, K.G., 2007. Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225 (4), 907
918. Kellermeier, F., Armengaud, P., Seditas, T.J., Danku, J., Salt, D.E., Amtmann, A., 2014. Analysis of the root system architecture of Arabidopsis provides a quantitative readout of crosstalk between nutritional signals. Plant Cell 26 (4), 1480
1496. Kelly, A.A., Froehlich, J.E., Do¨rmann, P., 2003. Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell 15 (11), 2694
2706. Khan, G.A., Bouraine, S., Wege, S., Li, Y., de Carbonnel, M., Berthomieu, P., et al., 2014. Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1;H3 in Arabidopsis. J. Exp. Bot. 65 (3), 871
884. Khorassani, R., Hettwer, U., Ratzinger, A., Steingrobe, B., Karlovsky, P., Claassen, N., 2011. Citramalic acid and salicylic acid in sugar beet root exudates solubilize soil phosphorus. BMC Plant Biol. 11 (1), 121
128. Kim, H.J., Lynch, J.P., Brown, K.M., 2008. Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant Cell Environ. 31 (12), 1744
1755. Kuo, H.F., Chiou, T.J., 2011. The role of microRNAs in phosphorus deficiency signaling. Plant Physiol. 156 (3), 1016
1024. Lambers, H., Finnegan, P.M., Laliberte´, E., Pearse, S.J., Ryan, M.H., Shane, M.W., et al., 2011. Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol. 156 (3), 1058
1066. Lambers, H., Clements, J.C., Nelson, M.N., 2013. How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am. J. Bot. 100 (2), 263
288. Lee, Y., Bak, G., Choi, Y., Chuang, W.I., Cho, H.T., Lee, Y., 2008. Roles of phosphatidylinositol 3-kinase in root hair growth. Plant Physiol. 147 (2), 624
635. Leggewie, G., Willmitzer, L., Riesmeier, J.W., 1997. Two cDNAs from potato are able to complement a phosphate uptake-deficient yeast mutant: identification of phosphate transporters from higher plants. Plant Cell 9 (3), 381
392. Lei, M., Liu, Y., Zhang, B., Zhao, Y., Wang, X., Zhou, Y., et al., 2011. Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis. Plant Physiol. 156 (3), 1116
1130.

Plant Life under Changing Environment

150

6. Regulation of low phosphate stress in plants

Lejay, L., Gansel, X., Cerezo, M., Tillard, P., Mu¨ller, C., Krapp, A., et al., 2003. Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell 15 (9), 2218
2232. Lejay, L., Wirth, J., Pervent, M., Cross, J.M.F., Tillard, P., Gojon, A., 2008. Oxidative pentose phosphate pathwaydependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol. 146 (4), 2036
2053. Li, M., Welti, R., Wang, X., 2006. Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol. 142 (2), 750
761. Li, Z., Gao, Q., Liu, Y., He, C., Zhang, X., Zhang, J., 2011. Overexpression of transcription factor ZmPTF1 improves low phosphate tolerance of maize by regulating carbon metabolism and root growth. Planta 233 (6), 1129
1143. Liang, C., Tian, J., Lam, H.M., Lim, B.L., Yan, X., Liao, H., 2010. Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiol. 152 (2), 854
865. Liang, G., He, H., Yu, D., 2012. Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One 7 (11), e48951. Liang, C., Wang, J., Zhao, J., Tian, J., Liao, H., 2014. Control of phosphate homeostasis through gene regulation in crops. Curr. Opin. Plant Biol. 21, 59
66. Liao, H., Yan, X., Rubio, G., Beebe, S.E., Blair, M.W., Lynch, J.P., 2004. Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct. Plant Biol. 31 (10), 959
970. Liu, H., Trieu, A.T., Blaylock, L.A., Harrison, M.J., 1998a. Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Mol. Plant Microbe Interact. 11 (1), 14
22. Liu, C., Muchhal, U.S., Uthappa, M., Kononowicz, A.K., Raghothama, K.G., 1998b. Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol. 116 (1), 91
99. Liu, J., Samac, D.A., Bucciarelli, B., Allan, D.L., Vance, C.P., 2005. Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J. 41 (2), 257
268. Liu, J., Magalhaes, J.V., Shaff, J., Kochian, L.V., 2009. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J. 57 (3), 389
399. Liu, F., Wang, Z., Ren, H., Shen, C., Li, Y., Ling, H.Q., et al., 2010. OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J. 62 (3), 508
517. Liu, T.Y., Lin, W.Y., Huang, T.K., Chiou, T.J., 2014a. MicroRNA-mediated surveillance of phosphate transporters on the move. Trends Plant Sci. 19 (10), 647
655. Liu, P., Chen, S., Song, A., Zhao, S., Fang, W., Guan, Z., et al., 2014b. A putative high affinity phosphate transporter, CmPT1, enhances tolerance to Pi deficiency of chrysanthemum. BMC Plant Biol. 14 (1), 18
38. Liu, J., Yang, L., Luan, M., Wang, Y., Zhang, C., Zhang, B., et al., 2015. A vacuolar phosphate transporter essential for phosphate homeostasis in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 112 (47), 6571
6578. Liu, F., Xu, Y., Jiang, H., Jiang, C., Du, Y., Gong, C., et al., 2016a. Systematic identification, evolution and expression analysis of the Zea mays PHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int. J. Mol. Sci. 17 (6), 930
955. Liu, T.Y., Huang, T.K., Yang, S.Y., Hong, Y.T., Huang, S.M., Wang, F.N., et al., 2016b. Identification of plant vacuolar transporters mediating phosphate storage. Nat. Commun. 7, 11095. Liu, B., Zhao, S., Wu, X., Wang, X., Nan, Y., Wang, D., et al., 2017. Identification and characterization of phosphate transporter genes in potato. J. Biotechnol. 264, 17
28. Liu, C., Su, J., Githengu, K.S., Wang, H., Song, A., Chen, F., et al., 2018a. Overexpression of phosphate transporter gene CmPht1;2 facilitated pi uptake and alternated the metabolic profiles of Chrysanthemum under phosphate deficiency. Front. Plant Sci. 9, e00686. Liu, F., Xu, Y., Han, G., Wang, W., Li, X., Cheng, B., 2018b. Identification and functional characterization of a maize phosphate transporter induced by mycorrhiza formation. Plant Cell Physiol. Available from: https:// doi.org/10.1093/pcp/pcy094. Lloyd, J.C., Zakhleniuk, O.V., 2004. Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J. Exp. Bot. 55 (400), 1221
1230.

Plant Life under Changing Environment

References

151

Lo´pez-Arredondo, D.L., Leyva-Gonza´lez, M.A., Gonza´lez-Morales, S.I., Lo´pez-Bucio, J., Herrera-Estrella, L., 2014. Phosphate nutrition: improving low-phosphate tolerance in crops. Ann. Rev. Plant Biol. 65 (1), 95
123. Lo´pez-Bucio, J., Herna´ndez-Abreu, E., Sa´nchez-Caldero´n, L., Nieto-Jacobo Ma, F., Simpson, J., Herrera-Estrella, L., 2002. Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol. 129 (1), 244
256. Lo´pez-Bucio, J., Herna´ndez-Abreu, E., Sa´nchez-Caldero´n, L., Pe´rez-Torres, A., Rampey, R.A., Bartel, B., et al., 2005. An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol. 137 (2), 681
691. Lota, F., Wegmuller, S., Buer, B., Sato, S., Brautigam, A., Hanf, B., et al., 2013. The cis-acting CTTC-P1BS module is indicative for gene function of LjVTI12, a Qb-SNARE protein gene that is required for arbuscule formation in Lotus japonicus. Plant J. 74 (2), 280
293. Loth-Pereda, V., Orsini, E., Courty, P.E., Lota, F., Kohler, A., Diss, L., et al., 2011. Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiol. 156 (4), 2141
2154. Lv, Q., Zhong, Y., Wang, Y., Wang, Z., Zhang, L., Shi, J., et al., 2014. SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. Plant Cell 26 (4), 1586
1597. Lynch, J.P., Brown, K.M., 2008. Root strategies for phosphorus acquisition. In: White, P.J., Hammond, J.P. (Eds.), The Ecophysiology of Plant-Phosphorus Interactions. Springer Netherlands, Dordrecht, pp. 83
116. Lynch, J.P., Ho, M.D., 2005. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269 (1), 45
56. Maeda, D., Ashida, K., Iguchi, K., Chechetka, S.A., Hijikata, A., Okusako, Y., et al., 2006. Knockdown of an arbuscular mycorrhizainducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol 47 (7), 807
817. Magalhaes, J.V., Liu, J., Guimaraes, C.T., Lana, U.G., Alves, V.M., Wang, Y.H., et al., 2007. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat. Genet. 39 (9), 1156
1161. Maharajan, T., Ceasar, S.A., Ajeesh Krishna, T.P., Ramakrishnan, M., Duraipandiyan, V., Naif Abdulla, A.D., et al., 2018. Utilization of molecular markers for improving the phosphorus efficiency in crop plants. Plant Breed. 137 (1), 10
26. Maldonado-Mendoza, I.E., Dewbre, G.R., Harrison, M.J., 2001. A phosphate transporter gene from the extraradical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol. Plant Microbe Interact. 14 (10), 1140
1148. Mekonnen, M.M., Hoekstra, A.Y., 2018. Global anthropogenic phosphorus loads to freshwater and associated grey water footprints and water pollution levels: a high-resolution global study. Water Res. Res. 54 (1), 345
358. Misson, J., Thibaud, M.C., Bechtold, N., Raghothama, K., Nussaume, L., 2004. Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol. Biol. 55 (5), 727
741. Mitsukawa, N., Okumura, S., Shirano, Y., Sato, S., Kato, T., Harashima, S., et al., 1997. Overexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions. Proc. Natl. Acad. Sci. U.S.A. 94 (13), 7098
7102. ´ ´ Młodzinska, E., Zboinska, M., 2016. Phosphate uptake and allocation-a closer look at Arabidopsis thaliana L. and Oryza sativa L. Front. Plant Sci. 7, e1198. Muchhal, U.S., Pardo, J.M., Raghothama, K.G., 1996. Phosphate transporters from the higher plant Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 93 (19), 10519
10523. Mudge, S.R., Rae, A.L., Diatloff, E., Smith, F.W., 2002. Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J. 31 (3), 341
353. Mu¨ller, R., Nilsson, L., Nielsen, L.K., Hamborg Nielsen, T., 2005. Interaction between phosphate starvation signalling and hexokinase-independent sugar sensing in Arabidopsis leaves. Physiol. Plant. 124 (1), 81
90. Mu¨ller, R., Morant, M., Jarmer, H., Nilsson, L., Nielsen, T.H., 2007. Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol. 143 (1), 156
171. Nacry, P., Canivenc, G., Muller, B., Azmi, A., Van Onckelen, H., Rossignol, M., et al., 2005. A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol. 138 (4), 2061
2074.

Plant Life under Changing Environment

152

6. Regulation of low phosphate stress in plants

Nagy, R., Karandashov, V., Chague, W., Kalinkevich, K., Tamasloukht, M., Xu, G.H., et al., 2005. The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J. 42 (2), 236
250. Nagy, R., Vasconcelos, M., Zhao, S., McElver, J., Bruce, W., Amrhein, N., et al., 2006. Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol. 8 (2), 186
197. Nakamori, K., Takabatake, R., Umehara, Y., Kouchi, H., Izui, K., Hata, S., 2002. Cloning, functional expression, and mutational analysis of a cDNA for Lotus japonicus mitochondrial phosphate transporter. Plant Cell Physiol. 43 (10), 1250
1253. Nakamura, Y., 2013. Phosphate starvation and membrane lipid remodeling in seed plants. Prog. Lipid Res. 52 (1), 43
50. Narang, R.A., Bruene, A., Altmann, T., 2000. Analysis of phosphate acquisition efficiency in different Arabidopsis accessions. Plant Physiol. 124 (4), 1786
1799. Nguyen, G.N., Rothstein, S.J., Spangenberg, G., Kant, S., 2015. Role of microRNAs involved in plant response to nitrogen and phosphorous limiting conditions. Front. Plant Sci. 6, e629. Nussaume, L., Kanno, S., Javot, H., Marin, E., Nakanishi, T.M., Thibaud, M.C., 2011. Phosphate import in plants: focus on the PHT1 transporters. Front. Plant Sci. 2, e83. Panigrahy, M., Rao, D.N., Sarla, N., 2009. Molecular mechanisms in response to phosphate starvation in rice. Biotechnol. Adv. 27 (4), 389
397. Pant, B.D., Buhtz, A., Kehr, J., Scheible, W.R., 2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 53 (5), 731
738. Pant, B.D., Musialak-Lange, M., Nuc, P., May, P., Buhtz, A., Kehr, J., et al., 2009. Identification of nutrientresponsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol. 150 (3), 1541
1555. Paszkowski, U., Kroken, S., Roux, C., Briggs, S.P., 2002. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 99 (20), 13324
13329. Paul, S., Datta, S.K., Datta, K., 2015. miRNA regulation of nutrient homeostasis in plants. Front. Plant Sci. 6, e232. Pedersen, B.P., Kumar, H., Waight, A.B., Risenmay, A.J., Roe-Zurz, Z., Chau, B.H., et al., 2013. Crystal structure of a eukaryotic phosphate transporter. Nature 496 (7446), 533
536. Pe´ret, B., Cle´ment, M., Nussaume, L., Desnos, T., 2011. Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci. 16 (8), 442
450. Pe´ret, B., Desnos, T., Jost, R., Kanno, S., Berkowitz, O., Nussaume, L., 2014. Root architecture responses: in search of phosphate. Plant Physiol. 166 (4), 1713
1723. Pe´rez-Torres, C.A., Lo´pez-Bucio, J., Cruz-Ramı´rez, A., Ibarra-Laclette, E., Dharmasiri, S., Estelle, M., et al., 2008. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20 (12), 3258
3272. Poirier, Y., Thoma, S., Somerville, C., Schiefelbein, J., 1991. Mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol. 97 (3), 1087
1093. Preuss, C.P., Huang, C.Y., Tyerman, S.D., 2011. Proton-coupled high-affinity phosphate transport revealed from heterologous characterization in Xenopus of barley-root plasma membrane transporter, HvPHT1;1. Plant Cell Environ. 34 (4), 681
689. Pudake, R.N., Mehta, C.M., Mohanta, T.K., Sharma, S., Varma, A., Sharma, A.K., 2017. Expression of four phosphate transporter genes from Finger millet (Eleusine coracana L.) in response to mycorrhizal colonization and Pi stress. 3 Biotech 7 (1), 17
29. Puga, M.I., Mateos, I., Charukesi, R., Wang, Z., Franco-Zorrilla, J.M., de Lorenzo, L., et al., 2014. SPX1 is a phosphate-dependent inhibitor of phosphate starvation response 1 in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 111 (41), 14947
14952. Rae, A.L., Cybinski, D.H., Jarmey, J.M., Smith, F.W., 2003. Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1 family. Plant Mol. Biol. 53 (1), 27
36. Raghothama, K.G., 1999. Phosphate acquisition. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50 (1), 665
693. Rausch, C., Bucher, M., 2002. Molecular mechanisms of phosphate transport in plants. Planta 216 (1), 23
37.

Plant Life under Changing Environment

References

153

Rausch, C., Daram, P., Brunner, S., Jansa, J., Laloi, M., Leggewie, G., et al., 2001. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414 (6862), 462
470. Remy, W., Taylor, T.N., Hass, H., Kerp, H., 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. U.S.A. 91 (25), 11841
11843. Rouached, H., Arpat, A.B., Poirier, Y., 2010. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol. Plant 3 (2), 288
299. Ryan, P., Delhaize, E., Jones, D., 2001. Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 527
560. Salazar-Vidal, M.N., Acosta-Segovia, E., Sa´nchez-Leo´n, N., Ahern, K.R., Brutnell, T.P., Sawers, R.J.H., 2016. Characterization and transposon mutagenesis of the maize (Zea mays) Pho1 gene family. PLoS One 11 (9), e0161882. Sasaki, T., Yamamoto, Y., Ezaki, B., Katsuhara, M., Ahn, S.J., Ryan, P.R., et al., 2004. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37 (5), 645
653. Schachtman, D.P., Reid, R.J., Ayling, S.M., 1998. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 116 (2), 447
453. Secco, D., Baumann, A., Poirier, Y., 2010. Characterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiol. 152 (3), 1693
1704. Secco, D., Wang, C., Arpat, B.A., Wang, Z., Poirier, Y., Tyerman, S.D., et al., 2012. The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol. 193 (4), 842
851. Secco, D., Jabnoune, M., Walker, H., Shou, H., Wu, P., Poirier, Y., et al., 2013. Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. Plant Cell 25 (11), 4285
4304. Secco, D., Shou, H., Whelan, J., Berkowitz, O., 2014. RNA-seq analysis identifies an intricate regulatory network controlling cluster root development in white lupin. BMC Genomics 15, 230. Sha, A.H., Wu, H., Fu, X.M., Zhang, Q.L., Guo, Q.L., Chen, Y.H., et al., 2014. Isolation and expression analysis of the soybean GmPic gene. Genet. Mol. Res. 13 (2), 4380
4391. Shane, M.W., McCully, M.E., Lambers, H., 2004. Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). J. Exp. Bot. 55 (399), 1033
1044. Shears, S.B., 2015. Inositol pyrophosphates: why so many phosphates? Adv. Biol. Regul. 57, 203
216. Shen, C., Wang, S., Zhang, S., Xu, Y., Qian, Q., Qi, Y., et al., 2013. OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativa L.). Plant Cell Environ. 36 (3), 607
620. Shi, S.L., Wang, D.F., Yan, Y., Zhang, F., Wang, H.D., Gu, M.S.S., 2013. Function of phosphate transporter OsPHT2;1 in improving phosphate utilization in rice. Chin. J. Rice Sci. 27, 457
465. Shimojima, M., Ohta, H., 2011. Critical regulation of galactolipid synthesis controls membrane differentiation and remodeling in distinct plant organs and following environmental changes. Prog. Lipid Res. 50 (3), 258
266. Shu, B., Xia, R.X., Wang, P., 2012. Differential regulation of Pht1 phosphate transporters from trifoliate orange (Poncirus trifoliata L. Raf) seedlings. Sci. Hortic 146, 115
123. Shukla, V., Kaur, M., Aggarwal, S., Bhati, K.K., Kaur, J., Mantri, S., et al., 2016. Tissue specific transcript profiling of wheat phosphate transporter genes and its association with phosphate allocation in grains. Sci. Rep. 6, 39293. Sisaphaithong, T., Kondo, D., Matsunaga, H., Kobae, Y., Hata, S., 2012. Expression of plant genes for arbuscular mycorrhiza-inducible phosphate transporters and fungal vesicle formation in sorghum, barley, and wheat roots. Biosci. Biotechnol. Biochem. 76 (12), 2364
2367. Smith, S., Gianinazzi-Pearson, V., 1988. Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39 (1), 221
244. Smith, S.E., Read, D. (Eds.), 2008. Mycorrhizal Symbiosis. third ed. Academic Press, London. Smith, S.E., Jakobsen, I., Grønlund, M., Smith, F.A., 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156 (3), 1050
1057. Song, H., Yin, Z., Chao, M., Ning, L., Zhang, D., Yu, D., 2014. Functional properties and expression quantitative trait loci for phosphate transporter GmPT1 in soybean. Plant Cell Environ. 37 (2), 462
472. Stefanovic, A., Arpat, A.B., Bligny, R., Gout, E., Vidoudez, C., Bensimon, M., et al., 2011. Over-expression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. Plant J. Cell Mol. Biol. 66 (4), 689
699.

Plant Life under Changing Environment

154

6. Regulation of low phosphate stress in plants

Stefanovic, A., Ribot, C., Rouached, H., Wang, Y., Chong, J., Belbahri, L., et al., 2007. Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. Plant J. Cell Mol. Biol. 50 (6), 982
994. Stetter, M.G., Benz, M., Ludewig, U., 2017. Increased root hair density by loss of WRKY6 in Arabidopsis thaliana. Peer J. 5, e2891. Su, T., Xu, Q., Zhang, F.C., Chen, Y., Li, L.Q., Wu, W.H., et al., 2015. WRKY42 modulates phosphate homeostasis through regulating phosphate translocation and acquisition in Arabidopsis. Plant Physiol. 167 (4), 1579
1591. Sun, H., Tao, J., Liu, S., Huang, S., Chen, S., Xie, X., et al., 2014. Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. J. Exp. Bot. 65 (22), 6735
6746. Sun, T., Li, M., Shao, Y., Yu, L., Ma, F., 2017. Comprehensive genomic identification and expression analysis of the phosphate transporter (PHT) gene family in apple. Front. Plant Sci. 8, e426. Svistoonoff, S., Creff, A., Reymond, M., Sigoillot-Claude, C., Ricaud, L., Blanchet, A., et al., 2007. Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. 39 (5), 792
797. Takabatake, R., Hata, S., Taniguchi, M., Kouchi, H., Sugiyama, T., Izui, K., 1999. Isolation and characterization of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice, and Arabidopsis. Plant Mol. Biol. 40 (3), 479
486. Tam, T.H.Y., Catarino, B., Dolan, L., 2015. Conserved regulatory mechanism controls the development of cells with rooting functions in land plants. Proc. Natl. Acad. Sci. U.S.A. 112, e3959
e3968. Tamura, Y., Kobae, Y., Mizuno, T., Hata, S., 2012. Identification and expression analysis of arbuscular mycorrhizainducible phosphate transporter genes of soybean. Biosci. Biotechnol. Biochem. 76 (2), 309
313. Teng, W., Zhao, Y.Y., Zhao, X.Q., He, X., Ma, W.Y., Deng, Y., et al., 2017. Genome-wide identification, characterization, and expression analysis of PHT1 phosphate transporters in wheat. Front. Plant Sci. 8, e543. Tian, J., Venkatachalam, P., Liao, H., Yan, X., Raghothama, K., 2007. Molecular cloning and characterization of phosphorus starvation responsive genes in common bean (Phaseolus vulgaris L). Planta 227 (1), 151
165. Ticconi, C.A., Lucero, R.D., Sakhonwasee, S., Adamson, A.W., Creff, A., Nussaume, L., et al., 2009. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc. Natl. Acad. Sci. U.S.A. 106 (33), 14174
14179. Tomscha, J.L., Trull, M.C., Deikman, J., Lynch, J.P., Guiltinan, M.J., 2004. Phosphatase under-producer mutants have altered phosphorus relations. Plant Physiol. 135 (1), 334
345. Valat, L., Degle`ne-Benbrahim, L., Kendel, M., Hussenet, R., Le Jeune, C., Schellenbaum, P., et al., 2018. Transcriptional induction of two phosphate transporter 1 genes and enhanced root branching in grape plants inoculated with Funneliformis mosseae. Mycorrhiza 28 (2), 179
185. Valdes-Lopez, O., Arenas-Huertero, C., Ramirez, M., Girard, L., Sanchez, F., Vance, C.P., et al., 2008. Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant Cell Environ. 31 (12), 1834
1843. Vance, C.P., Uhde-Stone, C., Allan, D.L., 2003. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol. 157 (3), 423
447. Vandamme, E., Renkens, M., Pypers, P., Smolders, E., Vanlauwe, B., Merckx, R., 2013. Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient Ferralsol. Plant Soil 369 (1/2), 269
282. Versaw, W.K., Harrison, M.J., 2002. A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14 (8), 1751
1766. Volpe, V., Giovannetti, M., Sun, X.G., Fiorilli, V., Bonfante, P., 2016. The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non mycorrhizal roots. Plant Cell Environ. 39 (3), 660
671. Walder, F., Brule´, D., Koegel, S., Wiemken, A., Boller, T., Courty, P.E., 2015. Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytol. 205 (4), 1632
1645. Waldie, T., McCulloch, H., Leyser, O., 2014. Strigolactones and the control of plant development: lessons from shoot branching. Plant J. 79 (4), 607
622. Wang, C., Yue, W., 2015. Rice SPX-Major Facility Superfamily3, a vacuolar phosphate efflux transporter, is involved in maintaining phosphate homeostasis in rice. Plant Physiol. 169 (4), 2822
2831. Wang, Y., Ribot, C., Rezzonico, E., Poirier, Y., 2004. Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol. 135 (1), 400
411. Wang, X., Wang, Y., Tian, J., Lim, B.L., Yan, X., Liao, H., 2009. Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiol. 151 (1), 233
240.

Plant Life under Changing Environment

References

155

Wang, G.Y., Shi, J.L., Ng, G., Battle, S.L., Zhang, C., Lu, H., 2011a. Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense. Mol. Plant 4 (3), 516
526. Wang, L., Li, Z., Qian, W., Guo, W., Gao, X., Huang, L., et al., 2011b. The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation. Plant Physiol. 157 (3), 1283
1299. Wang, C., Huang, W., Ying, Y., Li, S., Secco, D., Tyerman, S., et al., 2012. Functional characterization of the rice SPX-MFS family reveals a key role of OsSPX-MFS1 in controlling phosphate homeostasis in leaves. New Phytol. 196 (1), 139
148. Wang, J., Sun, J., Miao, J., Guo, J., Shi, Z., He, M., et al., 2013. A phosphate starvation response regulator Ta-PHR1 is involved in phosphate signalling and increases grain yield in wheat. Ann. Bot. 111 (6), 1139
1153. Wang, H., Xu, Q., Kong, Y.H., Chen, Y., Duan, J.Y., Wu, W.H., et al., 2014a. Arabidopsis WRKY45 transcription factor activates Phosphate Transporter1;1 expression in response to phosphate starvation. Plant Physiol. 164 (4), 2020
2029. Wang, S., Zhang, S., Sun, C., Xu, Y., Chen, Y., Yu, C., et al., 2014b. Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). New Phytol. 201 (1), 91
103. Wang, X., Wang, Y., Pin˜eros, M.A., Wang, Z., Wang, W., Li, C., et al., 2014c. Phosphate transporters OsPHT1;9 and OsPHT1;10 are involved in phosphate uptake in rice. Plant Cell Environ. 37 (5), 1159
1170. Wang, Z., Ruan, W., Shi, J., Zhang, L., Xiang, D., Yang, C., et al., 2014d. Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc. Natl. Acad. Sci. U.S.A. 111 (41), 14953
14958. Wang, F., Rose, T., Jeong, K., Kretzschmar, T., Wissuwa, M., 2016. The knowns and unknowns of phosphorus loading into grains, and implications for phosphorus efficiency in cropping systems. J. Exp. Bot. 67 (5), 1221
1229. Wege, S., Khan, G.A., Jung, J.Y., Vogiatzaki, E., Pradervand, S., Aller, I., et al., 2016. The EXS domain of PHO1 participates in the response of shoots to phosphate deficiency via a root-to-shoot signal. Plant Physiol. 170 (1), 385
400. Wegmu¨ller, S., Svistoonoff, S., Reinhardt, D., Stuurman, J., Amrhein, N., Bucher, M., 2008. A transgenic dTph1 insertional mutagenesis system for forward genetics in mycorrhizal phosphate transport of Petunia. Plant J. 54 (6), 1115
1127. Wild, R., Gerasimaite, R., Jung, J.Y., Truffault, V., Pavlovic, I., Schmidt, A., et al., 2016. Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science 352 (6288), 986
990. Wissuwa, M., Gamat, G., Ismail, A.M., 2005. Is root growth under phosphorus deficiency affected by source or sink limitations? J. Exp. Bot. 56 (417), 1943
1950. Wu, G., 2013. Plant microRNAs and development. J. Genet. Genomics 40 (5), 217
230. Xiao, K., Liu, J., Dewbre, G., Harrison, M., Wang, Z.Y., 2006. Isolation and characterization of root-specific phosphate transporter promoters from Medicago truncatula. Plant Biol. 8 (4), 439
449. Xie, X.A., Huang, W., Liu, F.C., Tang, N.W., Liu, Y., Lin, H., et al., 2013. Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis. New Phytol. 198 (3), 836
852. Xu, G.H., Chague, V., Melamed-Bessudo, C., Kapulnik, Y., Jain, A., Raghothama, K.G., et al., 2007. Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. J. Exp. Bot. 58 (10), 2491
2501. Xue, H.W., Chen, X., Mei, Y., 2009. Function and regulation of phospholipid signalling in plants. Biochem. J. 421 (2), 145
156. Yan, X., Liao, H., Beebe, S.E., Blair, M.W., Lynch, J.P., 2004. QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265 (1), 17
29. Yang, W.T., Baek, D., Yun, D.J., Hwang, W.H., Park, D.S., Nam, M.H., et al., 2014. Overexpression of OsMYB4P, an R2R3-type MYB transcriptional activator, increases phosphate acquisition in rice. Plant Physiol. Biochem. 80, 259
267. Ye, Y., Yuan, J., Chang, X., Yang, M., Zhang, L., Lu, K., et al., 2015. The phosphate transporter gene OsPht1;4 is involved in phosphate homeostasis in rice. PLoS One 10 (5), e0126186. Yi, K., Wu, Z., Zhou, J., Du, L., Guo, L., Wu, Y., et al., 2005. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol. 138 (4), 2087
2096. Zakhleniuk, O.V., Raines, C.A., Lloyd, J.C., 2001. pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh. Planta 212 (4), 529
534.

Plant Life under Changing Environment

156

6. Regulation of low phosphate stress in plants

Zeng, H.Q., Zhu, Y.Y., Huang, S.Q., Yang, Z.M., 2010. Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J. Plant Physiol. 167 (15), 1289
1297. Zhang, H., Huang, Y., Ye, X., Xu, F., 2011. Genotypic variation in phosphorus acquisition from sparingly soluble P sources is related to root morphology and root exudates in Brassica napus. Sci. China Life Sci. 54 (12), 1134
1142. Zhang, C., Meng, S., Li, M., Zhao, Z., 2016. Genomic identification and expression analysis of the phosphate transporter gene family in poplar. Front. Plant Sci. 7, e1398. Zhang, J., Guo, S., Ren, Y., Zhang, H., Gong, G., Zhou, M., et al., 2017. High-level expression of a novel chromoplast phosphate transporter ClPHT4;2 is required for flesh color development in watermelon. New Phytol. 213 (3), 1208
1221. Zhang, C., Simpson, R.J., Kim, C.M., Warthmann, N., Delhaize, E., Dolan, L., et al., 2018. Do longer root hairs improve phosphorus uptake? Testing the hypothesis with transgenic Brachypodium distachyon lines overexpressing endogenous RSL genes. New Phytol. 217 (4), 1654
1666. Zhao, L., Versaw, W.K., Liu, J., Harrison, M.J., 2003. A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelope. New Phytol. 157 (2), 291
302. Zhou, J., Jiao, F., Wu, Z., Li, Y., Wang, X., He, X., et al., 2008. OsPHR2 is involved in phosphatestarvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol. 146 (4), 1673
1686. Zhou, X., Huang, J., Zhou, Y., Shi, W., 2012. Genotypic variation of rape in phosphorus uptake from sparingly soluble phosphate and its active mechanism. Afr. J. Biotechnol. 11 (13), 3061
3069. Zhu, J., Lynch, J.P., 2004. The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Funct. Plant Biol. 31 (10), 949
958. Zhu, J., Kaeppler, S.M., Lynch, J.P., 2005. Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays). Funct. Plant Biol. 32 (8), 749
762. Zhu, W., Miao, Q., Sun, D., Yang, G., Wu, C., Huang, J., et al., 2012. The mitochondrial phosphate transporters modulate plant responses to salt stress via affecting ATP and gibberellin metabolism in Arabidopsis thaliana. PLoS One 7 (8), e43530.

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C H A P T E R

7 Regulation of flood stress in plants Yoonha Kim, Raheem Shahzad and In-Jung Lee Division of Plant Biosciences, School of Applied Biosciences, Kyungpook National University, Daegu, South Korea

7.1 Introduction Recently, agricultural climate has been rapidly changing due to increasing earth temperature, and as a result, crop cultivation land has been faced with serious environmental stresses, such as drought, salinity, thermo, ultraviolet (UV), ozone (O3), and flooding stress (Mall et al., 2004; Bailey-Serres et al., 2012). Among various environmental stresses, flooding stress is one of the major stresses which is caused by unexpected heavy precipitation during few hours or few days and it is being magnified as a main abiotic stress (BaileySerres et al., 2012; Kim et al., 2015; Loreti et al., 2016). According to English dictionary, flood(ing) is defined as “an overflow of water that submerges land which is usually dry.” Thus flooding stress in agricultural land is divided into two different types, one is waterlogging stress and the other is submergence stress, by the availability of water level to crops. Waterlogging stress is caused by the excess water contents in farming area so not only whole root area but also some parts of shoot are covered with water, while submergence stress means all plant parts are totally covered with water (Fig. 7.1). Therefore if plants are faced with both stress conditions (waterlogging and submergence), soil pores fill with water and these phenomena provoke serious physiological problems, such as photosynthesis (Bailey-Serres et al., 2012), hormonal imbalance (Kim et al., 2015), minerals uptake (Tamang and Fukao, 2015), limited gas diffusion (Nishiuchi et al., 2012), susceptibility to pests (Nguyen et al., 2012), and mitochondria respiration (Bailey-Serres and Voesenek, 2008; Nishiuchi et al., 2012) in plants. Thus flooding stress during crop cultivation causes enormous yield loss. In soybean cultivation, waterlogging stress induces significant yield loss depending on growth stage (vegetative stage: approximately 17% off; reproductive stage: approximately 50% off) (Nguyen et al., 2012). In corn cultivation, flooding stress during early growth stage (a height of 30 in.) for 24 and 96 hours induces 14% 30% yield loss (Ritter and Beer, 1969). In the case of cotton cultivation, waterlogging stress for 4 9 days causes 27% 30% yield loss (Wu et al., 2012). According to the FAO

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FIGURE 7.1 Glycolysis and metabolic pathway of ATP, NAD, and NAD(P) using the starch which is produced by photosynthesis. Plant can produce ATP, NAD, and NAD(P) regeneration through the multiple routes of sucrose catabolism. In the mitochondria respiration, pyruvate is a key intermediate of citric acid cycle. Pyruvate can convert to acetyl-CoA in the mitochondria under enough oxygen level, while pyruvate can convert to lactate or ethanol in the cytosol under oxygen limitation (anaerobic condition) which is shown in dotted line. Most of produced or regenerated energy (ATP and NADH) transport to photosynthetic reaction center, thus plant can activate photosynthesis process consistently. ATP, Adenosine triphosphate; NADH, nicotinamide adenine dinucleotide. Source: Modified from Kim, Y., 2019. Flooding tolerance mechanism in plants. J. Agric. Life Sci. 53 (2), 1 13.

report (2007), a lot of agricultural irrigated land areas (20 30 million hectares) are exposed to soil waterlogging due to poor soil drainage, intensive irrigation, and unexpected weather events (Najeeb et al., 2015). Moreover, approximately twice the size of the United States (17 million km2) is exposed to flooding stress and enormous flooding stress in all around the country, which causes damage costing of more than $80 billion (Perata et al., 2011). For this reason, many crop breeders have focused on the development of floodtolerant varieties or identification of flood-tolerant mechanism. Therefore several flooding tolerance varieties or accessions [Swarna-Sub1: rice (Dar et al., 2013), PI408105A: soybean (Nguyen et al., 2012), CAWL-46-3-1: maize (Zaidi et al., 2015), Ducula-4: wheat (vanGinkel et al., 1992)] have been developed, while on the other hand, specific genetic and biochemical mechanisms have also been identified in rice and other plants (Xu et al., 2006; BaileySerres and Voesenek, 2008; Nishiuchi et al., 2012; Nanjo et al., 2014; Kim et al., 2015). However, the vulnerability and tolerance mechanisms of various plants are different to

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flooding stress. Therefore, in this chapter, we will discuss about flooding tolerance strategies in crops and also will describe various tolerance or resistance mechanisms at genetic, biochemical, physiological, and morphological levels.

7.2 Plants strategies against flooding stress 7.2.1 Escape strategy under submergence Gaseous exchange between plants and their aerial environment is dramatically reduced when the water covers the soil pores during flooding stress because the diffusion of gases, such as O2, CO2, and gas hormone (ethylene), is very slow in water condition due to numerous barriers (Bailey-Serres and Voesenek, 2008). Thus the concentration of gases significantly reduces under flooding condition, so it can contribute to a lot of physiological problems, such as respiration of microorganisms and mitochondria in plants. Oxygen in soil is a necessity for respiration of plant root, so if the concentration of O2 is below its critical level (,10%) in soil, plants will face with hypoxia (partial O2 limitation) or anoxia (complete absence of O2) (Hodgson, 1982; Najeeb et al., 2015). It is well known, plants, by using carbon dioxide, water, and light via photosynthesis, produce carbon compounds, and photosynthesis is composed by light (thylakoid) and dark (stroma) reactions of the chloroplast. For constant photosynthesis reaction, plants need energy, such as adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide (NADH) (reduced form), to modulate photosystems I and II (Nelson and Yocum, 2006). In the plants, ATP and NADH are mainly supplied through citric acid cycle (CAC) during mitochondrial respiration (Millar et al., 2011). Precursor of CAC is known as an acetyl-CoA, which is produced from pyruvate by oxidizing via the pyruvate dehydrogenase complex (Millar et al., 2011) (Fig. 7.1). Citrate can sequently convert to isocitric acid, α-ketoglutaric acid, succinyl-CoA, succinic acid, fumaric acid, malic acid, and oxaloacetic acid by the help of several enzymes, such as citrate synthase, aconitase, isocitrate dehydrogenase, 2-oxoglutarate dehydrogenase, succinyl-CoA synthetase, succinate dehydrogenase, fumarase, and malate dehydrogenase, and consequently, plants can produce 2ATP, 6NADH, and 2FADH2 (total 24 ATP) (Rocha et al., 2010; Millar et al., 2011) (Fig. 7.1). All these processes occur in an aerobic condition; however, pyruvate cannot convert to acetyl-CoA in anaerobic condition, therefore pyruvate changes to lactate and ethanol via fermentation pathway (dotted line) (Rocha et al., 2010) (Fig. 7.1). Usually, studies related to submergence were conducted in subaquatic plants, such as rice. Even though rice plants are growing well under fresh water, most of the rice cultivars die within a week of complete submergence (Xu et al., 2006; Hattori et al., 2009). Among various rice cultivars, FR13A (Indica rice) cultivar showed resistance against the whole submerge condition for 2 weeks, so this cultivar was used as a parent line (tolerant) for developing quantitative trait locus (QTL) mapping population (Xu and Mackill, 1996). According to Xu et al. (2006), they produced mapping population (DX202), which was developed by a cross between IR40931-26 (indica, tolerant) and M-202 (japonica, intolerant), thereby identifying major QTLs involved in submergence tolerance in chromosome 9. According to their results, the involved gene in submergence tolerance was identified as a

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submergence 1 (Sub 1) (Xu et al., 2006). Flooding stress during rice cultivation at Southeast Asia can be classified into flash flooding (few weeks) and deepwater flooding (several months), depending on the stress exposure period or water depth (Jackson and Ram, 2003; Nishiuchi et al., 2012). If rice plants expose either flash flooding or deepwater flooding, these face severe metabolic problems due to low light and limited gaseous diffusion, and in addition, rice plants receive mechanical damage and increased invasion of pests and diseases (Ram et al., 1999). To escape submergence condition, deep rice plants endogenously accumulate growth hormone, gibberellin (GA), in the internode; it is modulated by SNORKEL1 (SK1) and SNORKEL2 (SK2) genes, which therefore triggers hyperelongated shoot (Hattori et al., 2009). Therefore some of the shoot parts rise above water level so that rice plant can supply oxygen from exposed leaves via developed aerenchyma cell (Hattori et al., 2009; Nishiuchi et al., 2012). More detailed physiological and genetic mechanisms will be discussed later.

7.2.2 Quiescence strategy under submergence As the plants are sessile and can’t avoid unfavorable environmental conditions, such as drought, salinity, thermo, UV, and water stress, so plants have evolved an adaptation or an evasion from various unfavorable environmental conditions. Flooding at agricultural land is caused by heavy rain during a short period. If plants face flash flooding due to heavy rain, most of the low-land rice select quiescence strategy to survive (Nishiuchi et al., 2012). In general, rice plants can survive for a couple of weeks under submergence, thus these endure complete submergence condition without any phenotypic changes. This phenomenon is known as quiescence strategy against submergence (Catling, 1992; Hattori et al., 2009; BaileySerres et al., 2012; Nishiuchi et al., 2012). These plants continuously grow to achieve oxygen above the water surface, therefore need a lot of energy for shoot. Because of this, rice plants show very weak growth recovery and poor pathogens resistance after water receding (Jackson and Ram, 2003). According to Setter and Laureles (1996), East Indian rice cultivar, FR13A, showed restricted shoot growth under submergence, and Fukao et al. (2006) revealed that FR13A saved energy during submergence; however, it is used energy for regrowing after desubmergence. For this reason, survival rate showed negative correlation with shoot length especially internode elongation (Setter and Laureles, 1996). As we mentioned previously, IR40931-26, which was inherited line from FR13A cultivar, was used for mapping population, and then three candidate loci (SUB1A, SUB1B, and SUB1C) were identified as SUB1 group (Xu and Mackill, 1996; Xu et al., 2006). All loci were identified as ethylene response factors (ERFs), but particularly, SUB1A is responsible for flash flooding (Xu et al., 2006; Nishiuchi et al., 2012). According to Fukao et al. (2006), accumulated SUB1A during flash flooding suppressed genes involved in α-amylase and sucrose synthase because these two are sources of sucrose and starch metabolism (Fig. 7.2).

7.2.3 Water logging tolerance strategy Water logging in farmland can be defined as root and some portion of the shoot submerging under water (Ahmed et al., 2013) (Fig. 7.2). Thus the main problem faced due to

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FIGURE 7.2 Different submergence tolerance mechanisms in rice plant. In the figure, quiescence strategy (left figure and black letter) means stop growing during flash flooding to save the carbohydrate because carbohydrate is a key energy source in the plant. Therefore preserve carbohydrates will be used for reactivating various physiological responses when plant extricates from submergence. These responses are caused by ethylene accumulation, and also SUB1A gene participates in the induction of quiescence response. Another submergence tolerance mechanism is called escape strategy (right figure and white letter). Escape strategy is very active response. If rice plant exposes to flooding rice plant recognize unfavorite condition via accumulation of endogenous ethylene, rice plants induce specific genes (SK1 and SK2) for accumulation of GA in the internode. Finally, accumulated GA induces hyper elongation of rice stem, thus some parts of stem are always exposure to atmosphere; therefore rice plant can supply oxygen from atmosphere to the root area through very well-developed lysigenous aerenchyma. GA, Gibberellin.

waterlogging is oxygen deficiency in rhizosphere, because most of the shoot parts are exposed to atmosphere in contrast with submergence (Ahmed et al., 2013; Nishiuchi et al., 2012; Kim et al., 2015). In general, field crops, such as soybean, wheat, and maize, are exposed to waterlogging due to unexpected heavy rain and poor drainage (Bailey-Serres and Voesenek, 2008; Perata et al., 2011; Nguyen et al., 2012; Wu et al., 2012). Waterlogging stress induces serious yield loss depending on crop growth stage (normally, reproductive stage showed more yield loss than vegetable stage) and environmental conditions, such as temperature, water turbidity, and a number of microbe (Nguyen et al., 2012; Kim et al., 2015). To survive or tolerate waterlogging, plants should develop some morphological changes or metabolic responses (Hossain and Uddin, 2011). In the case of soybean plants, adventitious roots are very well developed in shoot that is close to water surface during waterlogging (Fig. 7.2). When soybean plants are exposed to waterlogging, phenotypic changes, such as leaf wilting, shoot length, or shoot width, do not reveal for 1 2 days. However, shoot area close to water surface starts swelling after 4 6 days of waterlogging and then adventitious roots are emerged from swelled shoot (Fig. 7.2). Plant roots from inside also reveal a difference between normal growth condition and waterlogging condition. According to Kim et al. (2015), structurally well-organized cortex cell was measured in nonwaterlogging stress plant and, on the other hand, destroyed cortex cell, named “aerenchyma cell,” was detected in soybean plants growing under waterlogging condition. Under waterlogging condition, the soil condition would be regarded as a hypoxia; thus

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plants produce adventitious root and aerenchyma cell in the root to resist oxygen deficiency (Hossain and Uddin, 2011; Ahmed et al., 2013; Kim et al., 2015). In the case of wheat plants, waterlogging condition can drastically suppress seminal root growth. However, some waterlogging-tolerant genotypes showed constant seminal root growth (Huang et al., 1994; Hossain and Uddin, 2011). Therefore seminal root growth is also one of the tolerance responses. Wheat plants also produce aerenchyma cells in stem and root for adaptation to waterlogging conditions, and it is distinguished into lysigenous and schizogenous aerenchyma cells depending on the process of their formation (Evans, 2003; Visser and Voesenek, 2004; Hossain and Uddin, 2011). According to Haque et al. (2010), lysigenous aerenchyma cells are generated by cells death in the primary cortex cells in roots, whereas schizogenous aerenchyma cells are produced during cells separation; thus developmental process of schizogenous aerenchyma cells is accompanied by cells division and expansion (Jackson and Armstrong, 1999). Hence, more well-formed aerenchyma cells in wheat plants are able to resist waterlogging due to oxygen diffusion from shoot to root through aerenchyma cells (Hossain and Uddin, 2011). In the case of wetland plants, roots have a specific barrier between epidermis and exodermis or subepidermal layer to prevent oxygen loss from roots to rhizosphere, whereas nonwetland plants don’t have barrier for radial oxygen loss (ROL) or have partial barriers; hence, nonwetland plants diffuse a lot of oxygen from root (Jackson and Armstrong, 1999; Nishiuchi et al., 2012). According to Thomson et al. (1992), wheat plants can produce aerenchyma cells at adventitious roots to resist waterlogging condition; moreover, wheat plant formed ROL barriers partially in aerenchyma-developed root; thus only 20% of oxygen is consumed among total entering oxygen. On the other hand, waterlogging-tolerant wheat plants developed strong ROL barriers in aerenchyma cells in adventitious root; thus well-developed or more penetrated nodal root was revealed due to improved oxygen consumption (Thomson et al., 1992; Colmer et al., 1998).

7.3 Flooding tolerance mechanisms 7.3.1 Morphological response Under submergence condition, oxygen deficiency occurs in plants; thus plants respond morphologically to improve oxygen uptake. Most remarkable response is aerenchyma formation in the root cortex cell (Colmer et al., 1998; Seago et al., 2005; Striker et al., 2008; Striker, 2012; Kim et al., 2015). Thus formed aerenchyma cells provide oxygen continuously from aerial shoot to submerged roots. Hence, improved root growth and soil exploration are induced in plants under anaerobic conditions (Colmer and Pedersen, 2008; Striker, 2012). According to Seago et al. (2005), aerenchyma cells in the roots showed difference among plant genotypes. Moreover, four types of aerenchyma cells were distinguished by spatial arrangement of the aerenchyma tissue in plant roots, which were named graminaceous, cyperaceous, Apium, and Rumex, respectively (Justin and Armstrong, 1987). Monocotyledonous flowering plants, such as rice, wheat, and maize, are included in graminaceous type and this root type is similar to a bicycle wheel (Striker et al., 2007). Cyperus eragrostis Lam is included in

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cyperaceous group and this root type resembles a spider web (Justin and Armstrong, 1987). Lotus tenuis and Rumex crispus are included in Apium and Rumex types and the features of these root types are nonorganized structure and honeycomb, respectively (Striker et al., 2007). Each aerenchyma tissue is generated by different physiological responses, such as lysigeny, schizogeny, and expansigeny (Seago et al., 2005). The lysigeny is caused by breakdown and death of cells in the cortex zone and often coupled with cell separations during cells collapse. There are two distinguished patterns of lysigeny in plants. The first pattern is called radial lysigeny, which is caused by the destruction of cortex cells radially, so the shape of aerenchyma tissues looks like a bicycle wheel (Striker, 2012). The second pattern is caused by cells separation and extinguished in tangential sectors of the root cortex; thus these responses are called tangential lysigeny. Hence, shapes of aerenchyma tissues are very similar to a spider web (Striker, 2012). Reponses of schizogeny take place in cortex tissues by the expansion of intercellular spaces into lacunae along radial sectors to produce aerenchyma tissues. The expansigeny reaction induces the lacunae by cell enlargement and cell division without abolishing or any separation of cortex tissues (Striker, 2012). Other than aerenchyma tissue development, plants reveal other morphological differences in roots to survive flooding stress. Actually, plants can initiate adventitious roots when soil is covered with water (waterlogging and submergence) to get more oxygen or to uptake more nutrients (Kim et al., 2015). According to Jackson (2004), adventitious roots are generated or replaced by three different mechanisms in plant during flooding stress condition. First, adventitious roots are stimulated by preexisting root primordia located at shoot area. Second, a new root system is induced by initiation of root primordia. Third, roots, located at soil surface, are extended to woody and herbaceous species (Gibberd et al., 2001; Shimamura et al., 2007). So, plants can produce adventitious roots within relatively short term through the abovementioned mechanisms. According to Cox et al. (2004), to adapt or mitigate flooding stress, shoot parts also displayed some morphological changes in Rumex palustris during flooding stress. Flood-tolerant varieties, such as R. palustris, soybean (Glycine max), and rice (Oryza sativa), showed enhanced plant height than flood-intolerant varieties (Cox et al., 2004; Bailey-Serres and Voesenek, 2008; Heydarian et al., 2010; Kim et al., 2015). Most typical response is the increase in the petiole angle and this response is caused by very few hours. Next responses are increase of petiole length and leaf area above the water level, and all these responses are caused by plant hormonal modulation (GA) (Striker, 2012; Kim et al., 2015). Other shoot responses are called hypertrophy that looks like white spongy tissue, which are usually visible in stem near water surfaces (Shimamura et al., 2010). Hypertrophy tissues are secondary aerenchyma and are external forms of phellogen (Teakle et al., 2011) (Fig. 7.3). The main role of hypertrophy tissues in shoot is the improvement of oxygen movement between water and plant tissues to generate energy via mitochondria respiration (Teakle et al., 2011; Striker, 2012; Shimamura et al., 2014; Kim et al., 2015).

7.3.2 Endogenous hormonal response 7.3.2.1 Gibberellins The GAs comprised a large group of diterpenoid carboxylic acids, and up to now, 136 GAs have been identified in plants (Hedden and Thomas, 2012). Among them, only few

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FIGURE 7.3 Different root morphology in soybean (Glycine max) under waterlogging condition. In the left figure, root pictures are taken 10 days after waterlogging condition. Enormous adventitious roots are developed in soybean plant growing at waterlogging condition. In the figure, the red circle indicates adventitious roots. Adventitious roots are normally developed in the basal of stem and then, it dies when soil water drain out. You can see the dead adventitious roots as well as swelling stem (adventitious roots came from swelling stem) in the right picture (after blue arrow). Source: Modified from Seo, C.W., Lee, S.M., Kang, S.M., Park, Y.G., Kim, A.Y., Park, H. J., et al., 2017. Selection of suitable plant growth regulators for augmenting resistance to waterlogging stress in soybean plants (Glycine max L.). Korean J. Crop Sci. 62 (4), 325 332.

gases, such as GA1, GA3, GA4, and GA7, are considered biologically active forms of GAs (Hedden and Thomas, 2012; Kim et al., 2015, 2016). GAs can regulate various physiological responses, such as seed germination (Bewley, 1997), plant growth (Hedden and Thomas, 2012), flowering (Tata et al., 2016), and stress resistance (Hattori et al., 2009; Bailey-Serres et al., 2012). In general, GAs are main signaling molecules of plant growth regulation among various physiological responses because GA can stimulate not only plant cell size but also increase the number of plant cells (Jones and Kaufman, 1983; MacAdam et al., 1989; Goto and Pharis, 1999; Ueguchi-Tanaka et al., 2007; Colebrook et al., 2014). Thus reduction or increased GA levels and signaling contribute to growth restriction or growth promotion to avoid various unfavorite environmental conditions, such as cold, salinity, and osmotic stress (Colebrook et al., 2014). In particular, GAs are significantly involved in stress escape strategy under shading and submergence conditions (Colebrook et al., 2014). The ole of GA very well describes the deepwater rice under submergence condition (Hattori et al., 2009). Hattori et al. (2009) produced mapping population using two contrasting rice genotypes [Taichung65 (T65): short leaf and stem length, and C9285: deepwater rice], after that they identified specific QTL in chromosomes 1, 3, and 12. Among these the QTL on chromosome 12 revealed the most effective results for submergence; thus they produced nearly isogenic line 12 (NIL-12) to evaluate QTL effects. Through positional Plant Life under Changing Environment

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cloning and gain-of-function, two genes (SK1 and SK2) were identified and the genes induced hyper elongation of stem. According to Hattori et al. (2009), domain of SK genes showed high similarity to ERF of Arabidopsis (AtERF1) and O. sativa (OsERF1, OsSUB1A-1) and also these genes were expressed under submergence conditions in deepwater rice. Under submergence condition, ethylene production has significantly increased in deepwater and normal rice, while only SK1 and SK2 genes are expressed in deepwater rice (Xu et al., 2006; Hattori et al., 2009). In addition, both genes trigger the induction of hyper internode elongation because SK1 and SK2 induce accumulation of bioactive GA1 in deepwater rice (Hattori et al., 2009). To confirm correlation between GA and submergence, Hattori et al. (2009) applied GA biosynthesis inhibitor to deepwater rice, and then, they found suppressed stem growth. In the case of soybean plant, bioactive GA4 level showed difference between waterlogging-tolerant variety (PI408105A) and waterlogging susceptible variety (S99-2281) under waterlogging condition (Kim et al., 2015). In the PI408105A, GA4 content was significantly increased under waterlogging condition; on the other hand, GA4 level was significantly decreased in the S99-2281 as compared to nonstress condition (Fig. 7.4). According to Seo et al. (2017), exogenous application of GA4 induced hyper stem elongation; furthermore, it showed improved phenotypic data, such as chlorophyll content, chlorophyll fluorescence, and visual rating. All physiological or morphological responses against flooding stress were caused by increased endogenous bioactive GAs. 7.3.2.2 Ethylene Ethylene is a gaseous type of plant hormone and it induces various physiological responses, such as flowering, senescence, abscission, seed germination, triple response (thick, short, and curved), and stress responses (Van Doorn, 2002; Achard et al., 2007; Lin et al., 2009; Kim et al., 2015; Iqbal et al., 2017). In plants, methionine is a precursor of ethylene and it converts to intermediates, such as S-adenosylmethionine (AdoMet) and 1aminocyclopropane-1-carboxylic acid (ACC), by helping AdoMet synthetase, ACC synthase, and ACC oxidase (Arc et al., 2013). As we mentioned previously, intermediate ACC converts to ethylene through an oxidation, so oxygen is a key component to ethylene production (Arc et al., 2013; Kim et al., 2015). For this reason, if plants are exposed to flooding stress, ethylene production in plants root decreases due to the limitation of soil oxygen (anoxia and hypoxia), however, even if plants are exposed to flooding stress, plants show increased ethylene production due to the enhancement of ACC synthase (Dat et al., 2004). Other reason is that ethylene is gaseous type of plant hormone, thus ethylene easily accumulates because the diffusivity of ethylene is very slow in water (10,000 time slower than atmosphere) (Colmer and Flowers, 2008). Therefore increased ethylene can cue a perception of soil flooding, thus ethylene is significantly linked with combat strategy of plants against flooding stress (Dat et al., 2004; Xu et al., 2006; Bailey-Serres and Voesenek, 2008; Fukao and Bailey-Serres, 2008; Shimamura et al., 2014). Furthermore, accumulated ethylene participates in morphological changes, such as the development of adventitious roots (Yang et al., 2013) and aerenchyma cell formation, inside roots (De Klerk and Hanecakova, 2008) with and without other hormones (auxin and cytokinin). In addition, endogenous accumulation of auxin and ethylene triggers the development of adventitious roots for improving air diffusion through transportation channel in portion of stem and root (Visser et al., 1996). According to Kim et al. (2015), ethylene accumulation

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FIGURE 7.4 Endogenous GAs level in soybean plant under waterlogging condition. In the figure, WTL and WSL indicate waterlogging tolerance line and waterlogging susceptible line, respectively. Significantly increased GAs contents are measured in WTL as compared to WSL. In the figure, capital letter (A), (B), (C), (D) and (E) indicates non-bioactive or bioactive GAs in plants. GA4 (D), which is a bioactive GA and the others (A, B, C and E) are known as non-bioactive GA which is intermediates of bioactive GAs. These results indicated that endogenous GA also participates in waterlogging tolerance mechanism in soybean. This data was one of our research data and it was brought from previously published paper in Frontiers in Plant Science (Kim et al., 2015). GA, Gibberellin. Source: Adapted with permission from Kim, Y.H., Hwang, S.J., Waqas, M., Khan, A.L., Lee, J.H., Lee, J.D., et al., 2015. Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance. Front. Plant Sci. 6, 714.

induced the increase of lipid peroxidase (malondialdehyde); thus very well-developed aerenchyma cells were observed in waterlogging-tolerant soybean line than waterlogging susceptible soybean line. Waterlogging-tolerant soybean variety hereby improved air delivery between shoot and root area.

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7.3.2.3 Abscisic acid Precursor of abscisic acid (ABA) is known as carotenoid, and it converts into several intermediates, such as zeaxanthin, all-trans-violaxanthin, and neoxanthin, by the help of enzymes, such as zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase (Agrawal et al., 2001; Kim et al., 2014, 2016). So, biosynthesized ABA in plants can induce various physiological responses, such as regulation of water loss (stomatal closure), seed dormancy, and aerenchyma cell development, in roots (Shinozaki et al., 2003; Munns and Tester, 2008; Ollas et al., 2013; Shimamura et al., 2014). According to Shimamura et al. (2014), phellogen is a secondary meristem and it grows as cork tissues, which means dead cells with suberized walls. In the case of woody plants, secondary growth occurs among various dicot plants; thus the cork acts as a protective tissue after abolishing or damage of cortex in roots and shoots. Phellogen normally reveals in secondary aerenchyma, stems, roots, and root nodules when plants species, such as Sesbania rostrata, Melilotus siculus, and Viminaria juncea, are exposed to flooding condition (Walker et al., 1983; Shiba and Daimon, 2003; Teakle et al., 2011; Shimamura et al., 2014). In shoots and roots, white spongy tissues are called form of aerenchyma, and it is referred to as secondary aerenchyma (Shimamura et al., 2014). Thomas et al. (2005) and Shimamura et al. (2010) reported that secondary aerenchyma, which derived from phellogen in soybean plants, acted as an oxygen transfer channel from shoot and root tips, thus soybean plant showed resistance against flooding stress and all these responses were induced by ABA because ABA is involved in the induction of suberin biosynthesis and deposition in homologous cork tissues (Efetova et al., 2007). According to Shimamura et al. (2014), high concentration of ABA not only prevents suberin deposition in aerenchyma-developing portions but also induces the formation of secondary aerenchyma. Kim et al. (2015) also reported that waterlogging-tolerant variety showed significant decrease in endogenous ABA level as compared to waterlogging susceptible variety. They assumed that decreased ABA level produced more beneficial environment for producing aerenchyma cell in roots; therefore these physiological changes that were derived by ABA were one of the main resistance mechanisms against flooding stress. 7.3.2.4 Salicylic acid Salicylic acid (SA) also is regarded a plant hormone; thus it can participate various physiological responses, such as flowering, thermogenesis, ion absorption, programmed cell death (PCD), and stress resistance (Zhang et al., 2003; Yang et al., 2004; Brodersen et al., 2005). In particular, SA is significantly involved in biotic stress resistance, which means combat against insect or fugal invasion so these phenomena are including systemic acquired resistance and hypersensitive response (Yang et al., 2004). In plants and fungus, SA is biosynthesized by two different pathways, such as isochorismate synthase (ICS) and phenylalanine ammonia lyase, and most of the plants (approximately 95%) produce SA through ICS pathway. If plants are exposed to biotic stress due to fungal and insect attack, SA accumulates in neighbor cells from the attacked cells because high accumulation of SA can induce PCD to protect enemy invention. In the case of flooding stress, plants develop various types of aerenchyma tissue (graminaceous, cyperaceous, Apium, and Rumex) in root cells. As we mentioned in Section 7.3.1, graminaceous type was caused by collapse and death of cells in the cortex zone (Striker, 2012). According to Kim et al. (2015), waterlogging-tolerant soybean variety showed significantly increased SA level under waterlogging condition, and increased SA Plant Life under Changing Environment

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level can elucidate two reasons. First reason is that SA triggers PCD response in the root to develop aerenchyma tissue (graminaceous type) because the high level of SA induces lipid peroxidase. Second reason is that accumulated SA induces the development of adventitious root. Finally, increased SA induces the development of adventitious root and aerenchyma tissues in the root therefore improved oxygen uptake is possible.

7.3.3 Genetic response Plants have very sophisticated defense system, when plants face with submergence condition due to heavy rain, plants recognize that we need to operate defense mechanism. Flooding tolerance mechanisms are relatively well studied in rice plants. In the case of rice plants, they operate two different resistance mechanisms against submergence (Bailey-Serres and Voesenek, 2008; Striker, 2012). One is the quiescence strategy, which occurs in low-land rice during flash flooding and the other is escape strategy that happens in deepwater rice under deepwater-flooding condition (Bailey-Serres and Voesenek, 2008) (Fig. 7.2). The main difference between quiescence strategy and escape strategy is energy consumption under submergence. Low-land rice plants stop energy consumption, such as carbohydrate, after flash flooding because saved energy uses metabolic activity when water is drained out, while on the other hand, deepwater rice plants utilize much energy to produce a signal molecule, such as GA, and then, accumulated GA induces hyper elongation of internodes (Hattori et al., 2009). Of course, these responses are induced by accumulated ethylene production in both rice plants; however, both plants show different genetic responses (Xu et al., 2006; Hattori et al., 2009). In 2006 Sub1A gene was identified as a key gene related with submergence tolerance in rice (Xu et al., 2006). As we mentioned previously, Sub1A gene was detected by QTL mapping using contrasting parent lines against submergence, so Sub1 locus was mapped to an interval of 0.06 cM on chromosome 9 (Xu et al., 2006). According to Xu et al. (2006), Sub1 region physically spanned 182 kb which was between markers CR25K and SSR1A in submergence-tolerant rice genome, and it consisted of three genes containing ERF domains, designated Sub1A, Sub1B, and Sub1C, and 10 non-ERF genes including 4 transcribed etc. On the other hand, Sub1A region was absent in submergence susceptible rice genome, thus relatively short genome size (142 kb) was measured. Under submergence condition, tolerant rice plants revealed significantly upregulated Sub1A gene as compared to intolerant rice plants but Sub1B gene was less expressed in intolerant rice plants as compared to submergence-resistant rice plants (Xu et al., 2006). Therefore they hypothesized that Sub1A gene is a strong candidate to control submergence tolerance in deepwater rice. According to Perata and Voesenek (2007), the Sub1A gene conferred submergence tolerance by a quiescence strategy, which meant the repression of cell elongation and carbohydrate metabolism due to encoding ERF transcription factor. ERFs, such as SK1 and SK2, were reported, by Hattori et al. (2009), to be involved in rice adaptation in deepwater flooding condition, and these genes allow the rice plants adaptation in deep water by functioning as snorkels to supply air from the atmosphere to plant. The SK1 and SK2 genes were identified by QTL analysis combined with positional cloning, thus three major QTLs were detected on chromosomes 1, 3, and 12 (Hattori et al., 2009). Among these, chromosome 12 was considered the most effective one. So Hattori et al. (2009) produced NIL-12 to dissection of the genomic fragment on chromosome 12. Plant Life under Changing Environment

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According to their results, SK1 and SK2 include a putative nuclear localization signal and a single APETALA2/ERF domain; thus it was categorized as belonging to the ERF subfamily (Hattori et al., 2009). Furthermore, they also conducted evolution test of SK genes by using wild rice species, such as Oryza rufipogon (W0120) and Oryza nivara (W0106), and their results showed that W0120 responded dramatically to deepwater condition (elongated internodes), while, on the other hand, W0106 showed little response against deepwater condition. Consequently, they compared sequence of the SK genes in W0120 and W0106. According to the results, W0120 had both genes, while W0106 had SK1 gene and a new stop codon in exon 2 of SK2 by insertion of a transposon (Hattori et al., 2009). Same stop codon was detected in other accessions of O. nivara as well. Therefore their results indicated that SK2 has a more pronounced effect than SK1 through the gain-of-function analysis.

7.4 Conclusion Plants are sessile and cannot escape from local changing environment, thus plants alter different defense mechanisms to cope with unfavorite environmental condition, such as flooding stress. Therefore a thorough understanding of how plants sense and respond to flooding stress is needed. The semiaquatic plants, such as rice, have been evolved to adapt the flooding condition; thus we recognize the detail mechanism of flooding resistance in rice plant through genetic, enzymatic, and biochemical studies and concluded that ERF is a key component of flooding tolerance mechanism. Increased ERF factors, such as SUB1 and SK1, induce different physiological responses. Increased SUB1 gene reduces energy consuming for stop growing, while SK1 gene stimulates accumulation of bioactive GA in the stem for rapid shoot growth. In the case of terrestrial plants, such as soybean, maize, cotton, and barely, accurate resistance or avoidance mechanism has not yet been identified at field condition. According to researchers, using contrast germplasms against flooding and waterlogging conditions, accumulation of ethylene are known as a major difference in soybean and maize. Therefore tolerant crops can induce various morphological attributes, such as development of adventitious root, aerenchyma cell formation, and different root architecture (number of later root, area, and angle). Furthermore, another plant hormones (ABA and SA) and antioxidants (catalase, CAT; glutathione, GSH; ascorbate peroxidase, APX) also significantly participate in stress mitigation via downregulation of reactive oxygen species or reactive nitrogen species. In conclusion, the flooding tolerance of crop plants is due to their diversely complex responses. In spite of complication, relatively detailed mechanisms are identified in rice plants, so many scientists are trying to identify flooding tolerance mechanism in terrestrial plants (major field crop). In spite of their efforts, major mechanisms have not yet been identified due to various environmental factors. Therefore it is recommend to focus on other factors, such as soil borne disease or other circumstance condition, to unearth some major factors during flooding condition.

Acknowledgment This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2017R1D1A3B03030917).

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References Achard, P., Baghour, M., Chapple, A., Hedden, P., Van Der Straeten, D., Genschik, P., et al., 2007. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc. Natl. Acad. Sci. U.S.A. 104 (15), 6484 6489. Agrawal, G.K., Yamazaki, M., Kobayashi, M., Hirochika, R., Miyao, A., Hirochika, H., 2001. Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion. Tagging of a zeaxanthin epoxidase gene and a novel OsTATC gene. Plant Physiol. 125, 1248 1257. Ahmed, F., Rafii, M.Y., Ismail, M.R., Juraimi, A.S., Rahim, H.A., Asfaliza, R., et al., 2013. Waterlogging tolerance of crops: breeding, mechanism of tolerance, molecular approaches, and future prospects. BioMed Res. Int. 2013, ID9635254. Arc, E., Sechet, J., Corbineau, F., Rajjou, L., Marion-Poll, A., 2013. ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front. Plant Sci. 4, 63. Available from: https://doi.org/10.3389/ fpls.2013.00063. Bailey-Serres, J., Voesenek, L.A.C.J., 2008. Flooding stress: acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313 339. Bailey-Serres, J., Fukao, T., Gibbs, D.J., Holdsworth, M.J., Lee, S.C., Licausi, F., et al., 2012. Making sense of low oxygen sensing. Trends Plant Sci. 17, 129 138. Bewley, J.D., 1997. Seed germination and dormancy. Plant Cell 9, 1055 1066. Brodersen, P., Malinovsky, F.G., He´maty, K., Newman, M.A., Mundy, J., 2005. The role of salicylic acid in the induction of cell death in Arabidopsis acd11. Plant Physiol. 138, 1037 1045. Catling, D., 1992. Rice in Deep Water. MacMillan Press, London. Colmer, T.D., Flowers, T.J., 2008. Flooding tolerance in halophytes. New Phytol. 179, 964 974. Colmer, T.D., Pedersen, O., 2008. Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange. New Phytol. 177, 918 926. Colmer, T.D., Gibbered, M.R., Wiengweera, A., Tinh, T.K., 1998. The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. J. Exp. Bot. 49, 1431 1436. Cox, M.C.H., Benschop, J.J., Vreeburg, R.A.M., Wagemaker, C.A.M., Moritz, T., Peeters, A.J.M., et al., 2004. The roles of ethylene, auxin, abscisic acid, and gibberellin in the hyponastic growth of submerged Rumex palustris petioles. Plant Physiol. 136, 2948 2960. Dat, J.F., Capelli, N., Folzer, H., Bourgeade, P., Badot, P.M., 2004. Sensing and signaling during plant flooding. Plant Physiol. Biochem. 42, 273 282. Dar, M.H., de Janvry, A., Emerick, K., Raitzer, D., Sadoulet, E., 2013. Flood-tolerant rice reduces yield variability and raises expected yield, differentially benefitting socially disadvantaged groups. Sci. Rep. 3, 3315. Available from: https://doi.org/10.1038/srep03315. De Klerk, G.J., Hanecakova, J., 2008. Ethylene and rooting of mung bean cuttings. The role of auxin induced ethylene synthesis and phase-dependent effects. Plant Growth Regul. 56, 203 209. Colebrook, E.H., Thomas, S.G., Phillips, A.L., Hedden, P., 2014. The role of gibberellins signaling in plant responses to abiotic stress. J. Exp. Biol. 217, 67 75. Efetova, M., Zeier, J., Riederer, M., Lee, C.W., Stingl, N., Mueller, M., et al., 2007. A central role of abscisic acid in drought stress protection of Agrobacterium-induced tumors on Arabidopsis. Plant Physiol. 145, 853 862. Evans, D.E., 2003. Aerenchyma formation. New Phytol. 161, 35 49. Fukao, T., Bailey-Serres, J., 2008. Ethylene—a key regulator of submergence responses in rice. Plant Sci. 175, 43 51. Fukao, T., Xu, K., Ronald, P.C., Bailey-Serres, J., 2006. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18, 2021 2034. Gibberd, M.R., Gray, J.D., Cocks, P.S., Colmer, T.D., 2001. Waterlogging tolerance among a diverse range of Trifolium accessions is related to root porosity, lateral root formation and aerotropic rooting. Ann. Bot. 88, 579 589. Goto, N., Pharis, R.P., 1999. Role of gibberellins in the development of floral organs of the gibberellin-deficient mutant, ga1-1, of Arabidopsis thaliana. Can. J. Bot. 77 (7), 944 954. Haque, M.E., Abe, F., Kawaguchi, K., 2010. Formation and extension of lysigenous aerenchyma in seminal root cortex of spring wheat (Triticum aestivum cv. Bobwhite line SH9826) seedlings under different strength of water logging. Plant Root 4, 31 39.

Plant Life under Changing Environment

References

171

Hattori, Y., Nagai, K., Furukawa, S., Song, X.J., Kawano, R., Sakakibara, H., et al., 2009. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460 (7258), 1026 1030. Hedden, P., Thomas, S.G., 2012. Gibberellin biosynthesis and its regulation. Biochem. J. 444 (1), 11 25. Heydarian, Z., Sasidharan, R., Cox, M.C.H., Pierik, R., Voesenek, L.A.C.J., Peeters, A.J.M., 2010. A kinetic analysis of hyponastic growth and petiole elongation upon ethylene exposure in Rumex palustris. Ann. Bot. 106, 429 435. Hodgson, A.S., 1982. The effects of duration, timing and chemical amelioration of short-term water logging during furrow irrigation of cotton in a cracking grey clay. Aust. J. Agric. Res. 33, 1019 1028. Hossain, A., Uddin, S.N., 2011. Mechanisms of waterlogging tolerance in wheat: morphological and metabolic adaptations under hypoxia or anoxia. Aust. J. Crop Sci. 5 (9), 1094 1101. Huang, B., Johnson, J.W., Nesmith, D.S., Bridges, D.C., 1994. Root and shoot growth of wheat genotypes in response to hypoxia and subsequent resumption of aeration. Crop Sci. 34, 1538 1544. Iqbal, N., Khan, N.A., Ferrante, A., Trivellini, A., Francini, A., Khan, M.I.R., 2017. Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front. Plant Sci. 8, 475. Jackson, M.B., 2004. The impact of flooding stress on plants and crops. ,http://www.plantstress.com/articles/ waterlogging_i/waterlog_i.htm.. Jackson, M.B., Armstrong, W., 1999. Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol. 1, 274 287. Jackson, M.B., Ram, P.C., 2003. Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann. Bot. 91, 227 241. Jones, R.L., Kaufman, P.B., 1983. The role of gibberellins in plant cell elongation. Crit. Rev. Plant Sci. 1 (1), 23 47. Justin, S.H.F.W., Armstrong, W., 1987. The anatomical characteristics of roots and plant response to soil flooding. New Phytol. 106, 465 495. Kim, Y.H., Khan, A.L., Waqas, M., Shim, J.K., Kim, D.H., Lee, K.Y., et al., 2014. Silicon application to rice root zone influenced the phytohormonal and antioxidant responses under salinity stress. J. Plant Growth Regul. 33, 137 149. Kim, Y.H., Hwang, S.J., Waqas, M., Khan, A.L., Lee, J.H., Lee, J.D., et al., 2015. Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance. Front. Plant Sci. 6, 714. Kim, Y.H., Khan, A.L., Lee, I.J., 2016. Silicon: a duo synergy for regulating crop growth and hormonal signaling under abiotic stress condition. Crit. Rev. Biotechnol. 36 (6), 1099 1109. Lin, Z., Zhong, S., Grierson, D., 2009. Recent advances in ethylene research. J. Exp. Bot. 60 (12), 3311 3336. Loreti, E., van Veen, H., Perata, P., 2016. Plant responses to flooding stress. Curr. Opin. Plant Biol. 33, 64 71. MacAdam, J.W., Volenec, J.J., Nelson, C.J., 1989. Effects of nitrogen on mesophyll cell division and epidermal cell elongation in tall fescue leaf blades. Plant Physiol. 89 (2), 549 556. Mall, R.K., Lal, M., Bhatia, V.S., Rathore, L.S., Singh, R., 2004. Mitigating climate change impact on soybean productivity in India: a simulation study. Agric. For. Meteorol. 121, 113 125. Millar, A.H., Whelan, J., Soole, K.L., Day, D.A., 2011. Organization and regulation of mitochondrial respiration in plants. Annu. Rev. Plant Biol. 62, 79 104. Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651 681. Najeeb, U., Bange, M.P., Tan, D.K., Atwell, B.J., 2015. Consequences of waterlogging in cotton and opportunities for mitigation of yield losses. AoB Plants 7, plv080. Available from: https://doi.org/10.1093/aobpla/plv080. Nanjo, Y., Jang, H.Y., Kim, H.S., Hiraga, S., Woo, S.H., Komatsu, S., 2014. Analyses of flooding tolerance of soybean varieties at emergence and varietal differences in their proteomes. Phytochemistry 106, 25 36. Nelson, N., Yocum, C.F., 2006. Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57, 521 565. Nguyen, V.T., Vuong, T.D., VanToai, T., Lee, J.D., Wu, X., Rouf Mian, M.A., et al., 2012. Mapping of quantitative trait loci associated with resistance to Phytophthora sojae and flooding tolerance in soybean. Crop Sci. 52, 2481 2493. Nishiuchi, S., Yamauchi, T., Takahashi, H., Kotula, L., Nakazono, M., 2012. Mechanisms for coping with submergence and waterlogging in rice. Rice 5 (1), 2. Ollas, C., Hernando, B., Arbona, V., Go´mez-Cadenas, A., 2013. Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol. Plant. 147, 296 306.

Plant Life under Changing Environment

172

7. Regulation of flood stress in plants

Perata, P., Voesenek, L.A.C.J., 2007. Submergence tolerance in rice requires Sub1A, an ethylene-response-factorlike gene. Trends Plant Sci. 12, 43 46. Perata, P., Armstrong, W., Voesenek, L.A., 2011. Plants and flooding stress. New Phytol. 190, 269 273. Ram, P.C., Singh, A.K., Singh, B.B., Singh, V.K., Singh, H.P., Setter, T.L., et al., 1999. Environmental characterization of floodwater in eastern India: relevance to submergence tolerance of lowland rice. Exp. Agric. 35, 141 152. Ritter, W.F., Beer, C.E., 1969. Yield reduction by controlled flooding of corn. Trans. ASAE 12, 46 50. Rocha, M., Licausi, F., Arau´jo, W.L., Nunes-Nesi, A., Sodek, L., Fernie, A.R., et al., 2010. Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicas. Plant Physiol. 152, 1501 1513. Seago, J.L., Marsh, L.C., Stevens, K.J., Soukup, A., Vortubova´, O., Enstone, D.E., 2005. A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Ann. Bot. 96, 565 579. Seo, C.W., Lee, S.M., Kang, S.M., Park, Y.G., Kim, A.Y., Park, H.J., et al., 2017. Selection of suitable plant growth regulators for augmenting resistance to waterlogging stress in soybean plants (Glycine max L.). Korean J. Crop Sci. 62 (4), 325 332. Setter, T.L., Laureles, E.V., 1996. The beneficial effect of reduced elongation growth on submergence tolerance of rice. J. Exp. Bot. 47, 1551 1559. Shiba, H., Daimon, H., 2003. Histological observation of secondary aerenchyma formed immediately after flooding in Sesbania cannabina and S. rostrata. Plant Soil 255, 209 215. Shimamura, S., Yoshida, S., Mochizuki, T., 2007. Crtical aerenchyma formation in hypocotyl and adventitious roots of Luffa cylindrical subjected to soil flooding. Ann. Bot. 100, 1431 1439. Shimamura, S., Yamamoto, R., Nakamura, T., Shimada, S., Komatsu, S., 2010. Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Ann. Bot. 106, 277 284. Shimamura, S., Yoshioka, T., Yamamoto, R., Hiraga, S., Nakamura, T., Shimada, S., et al., 2014. Role of abscisic acid in flood-induced secondary aerenchyma formation in soybean (Glycine max) hypocotyls. Plant Prod. Sci. 17, 131 137. Shinozaki, K., Yamaguchi-Shinozaki, K., Seki, M., 2003. Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant Biol. 6, 410 417. Striker, G.G., 2012. Flooding stress on plants: anatomical, morphological and physiological responses. In Botany. InTech. Striker, G.G., Insausti, P., Grimoldi, A.A., Vega, A.S., 2007. Trade-off between root porosity and mechanical strength in species with different types of aerenchyma. Plant Cell Environ. 30, 580 589. Striker, G.G., Insausti, P., Grimoldi, A.A., 2008. Flooding effects on plant recovery from defoliation in the grass Paspalum dilatatum and the legume Lotus tenuis. Ann. Bot. 102, 247 254. Tamang, B.G., Fukao, T., 2015. Plant adaptation to multiple stresses during submergence and following desubmergence. Int. J. Mol. Sci. 16, 30164 30180. Tata, S.K., Jung, J., Kim, Y.H., Choi, J.Y., Jung, J.Y., Lee, I.J., et al., 2016. Heterologous expression of chloroplastlocalized geranylgeranyl pyrophosphate synthase confers fast plant growth, early flowering and increased seed yield. Plant Biotechnol. J. 14, 29 39. Teakle, N.L., Armstrong, J., Barrett Lennard, E.G., Colmer, T.D., 2011. Aerenchymatous phellem in hypocotyl and roots enables O2 transport in Melilotus siculus. New Phytol. 190, 340 350. Thomas, A.L., Guerreiro, S.M.C., Sodek, L., 2005. Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Ann. Bot. 96, 1191 1198. Thomson, C.J., Colmer, T.D., Watkin, E.L.J., Greenway, H., 1992. Tolerance of wheat (Triticum aestivum cv. Gamenya and Kite) and triticale (Triticosecale cv. Muir) to waterlogging. New Phytol. 120, 335 344. Ueguchi-Tanaka, M., Nakajima, M., Motoyuki, A., Matsuoka, M., 2007. Gibberellin receptor and its role in gibberellin signaling in plants. Annu. Rev. Plant Biol. 58, 183 198. Van Doorn, W.G., 2002. Effect of ethylene on flower abscission: a survey. Ann. Bot. 89, 689 693. vanGinkel, M., Rajaram, S., Thijssen, M., 1992. Waterlogging in wheat: germplasm evaluation and methodology development. The Seventh Wheat Workshop for Eastern. Central and Southern Africa, Nakuru, Kenya, pp. 115 124, 16 19 September 1991. Visser, E.J.W., Voesenek, L.A.C.J., 2004. Acclimation to soil flooding—sensing and signal—transduction. Plant Soil 254, 197 214.

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Further reading

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Visser, E., Cohen, J.D., Barendse, G., Blom, C., Voesenek, L., 1996. An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm. Plant Physiol. 112, 1687 1692. Walker, B.A., Pate, J.S., Kuo, J., 1983. Nitrogen fixation by nodulated roots of Viminaria juncea (Schrad. & Wendl.) Hoffmans, (Fabaceae) when submerged in water. Aust. J. Plant Physiol. l10, 409 421. Wu, Q.X., Zhu, J.Q., Liu, K.W., Guo, C.L., 2012. Effects of fertilization on growth and yield of cotton after surface waterlogging elimination. Adv. J. Food Sci. Technol. 4, 398 403. Xu, K., Mackill, D.J., 1996. A major locus for submergence tolerance mapped on rice chromosome 9. Mol. Breed. 2, 219 224. Xu, K., Xu, X., Fukao, T., Canlas, P., Maghirang-Rodriguez, R., Heuer, S., et al., 2006. Sub1A is an ethyleneresponse-factor-like gene that confers submergence tolerance to rice. Nature 442, 705 708. Yang, Y., Qi, M., Mei, C., 2004. Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J. 40, 909 919. Yang, W., Zhu, C., Ma, X., Li, G., Gan, L., Ng, D., et al., 2013. Hydrogen peroxide is a second messenger in the salicylic acid-triggered adventitious rooting process in mung bean seedlings. PLoS One 27 8 (12), e84580. Zaidi, P.H., Rashid, Z., Vinayan, M.T., Almeida, G.D., Phagna, R.K., Babu, R., 2015. QTL mapping of agronomic waterlogging tolerance using recombinant inbred lines derived from tropical maize (Zea mays L) germplasm. PLoS One 10 (4), e0124350. Zhang, Y., Chen, K., Zhang, S., Ferguson, I., 2003. The role of salicylic acid in post harvest ripening of kiwi fruit. Post Harvest Biol. Technol. 28, 67 74.

Further reading Armstrong, W., Cousins, D., Armstrong, J., Turner, D.W., Beckett, P.M., 2000. Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis. Ann. Bot. 86, 687 703.

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C H A P T E R

8 Heavy metals, water deficit, and their interaction in plants: an overview Mamta Hirve1, Meeta Jain1, Anshu Rastogi2 and Sunita Kataria1 1

School of Biochemistry, Devi Ahilya University, Indore, India 2Laboratory of Bioclimatology, Department of Ecology and Environmental Protection, Poznan University of ´ Poland Life Sciences, Poznan,

8.1 Introduction Due to its sessile nature, plants are in continuous exposure to different abiotic stresses in nature. The cooccurrence of multiple abiotic-stress conditions is very frequent in the field environment (Suzuki et al., 2014). The major environmental stress factors include heavy-metal toxicity, drought or water deficit, heat, cold, nutrient deficiency, freezing, ozone, salinity, chilling, and high light intensity (Nakashima and Yamaguchi-Shinozaki, 2006; Agarwal and Grover, 2006; Hirel et al., 2007; Kalaji et al., 2018). Among these abiotic stresses, heavy metal and water deficit are two different abiotic constraints that affect normal growth and metabolism of the plant. The outcome of the concurrent occurrence of these two stresses is their interaction and a several fold increase in complexity in plant responses (Suzuki et al., 2014). Although considerable research on heavy metal and water deficit as individual stresses have been done, studies with simultaneous exposure of these two stresses are very few in the available literature. In recent times, work has started to uncover physiological responses as well as molecular mechanisms of plant encountering the combinations of these stresses. A group of metals or metalloids defines the heavy metals, when its atomic density exceeds 4 g/cm3 or is five times higher when compared with water (Hawkes, 1997). Heavy metal elements include cadmium (Cd), silver (Ag), nickel (Ni), lead (Pb), cobalt (Co), zinc (Zn), iron (Fe), manganese (Mn), arsenic (As), chromium (Cr) and the platinum group elements (Nagajyoti et al., 2010). The heavy metals released from industries and urbanization often contaminate the agricultural soil. The heavy metals are introduced into the environment by various sources including organic

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wastes, combustion of fuels, industrial effluents, refuse burning, improper agricultural practices, transport, and power generation (Caglieri et al., 2006). 45% of the agricultural area is continuously exposed to water deficiency, resulting in a global loss of 50% of the total yield per year (Abdelrahman et al., 2017). The receptiveness of plants to water-deficit stress is influenced by the plant species, the degree of stresses, and the developmental stage of a plant (Demirevska et al., 2009). In nature, both abiotic and biotic stresses occur simultaneously in different degrees of their combinations. This chapter discusses the impact of heavy metals, water deficit, and their interaction in plants.

8.2 Heavy-metal effects on plants The occurrence of heavy metals in agricultural soil causes different artifacts in plant growth and metabolism and impacts different biochemical and physiological processes of the plants (Nagajyoti et al., 2010). Among different metals, Cu, Mo, Co, Ni, Mn, Fe, and Zn are trace elements required by plants in small quantity for normal growth and are therefore considered to be essential micronutrients (Reeves and Baker, 2000). They mainly act as cofactors for several vital metabolic enzymes, but when present in them cause a harmful impact on plants (Monni et al., 2000). Cr, Cd, Pb, As, etc., are other heavy metals, which are not required by plants for their normal growth and are therefore considered as nonessential elements; a very low concentration of these elements may cause deleterious effects on plants (Emamverdian et al., 2015). Despite essentiality and nonessentiality, metal elements, which are immobilized in plant tissues, are considered more hazardous and the most detrimental metals to crops; these are Zn, Pb, Ni, Cd, Mo, and Cu (Lasat, 2002).

8.2.1 Essential heavy-metal elements 8.2.1.1 Copper Copper as a trace element is a part of plant’s structural and regulatory proteins, which takes part in various metabolic processes, including respiration and photosynthesis (Demirevska-kepova et al., 2004), oxidative stress response (Martinez-Penalver et al., 2012), as well as in hormone signaling and cell wall metabolism (Pilon et al., 2006). It is mainly located in the cytosol, thylakoid lumen, chloroplast stroma, endoplasmic reticulum, apoplast, and mitochondria of the plant cell. Plastocyanin and copper/zinc superoxide dismutase are the major Cu-containing proteins in plants (Marschner, 1995). Other proteins include ethylene receptors, cytochrome-C oxidase, and various apoplastic oxidases, such as ascorbate oxidase, diamine oxidase, and polyphenol oxidase (Pilon et al., 2006). Cu at high levels becomes strongly phytotoxic, causing inhibition of seed germination, root and shoot length, ratio of root-to-shoot, and dry weight accumulation. Necrosis and chlorosis due to the reduction of growth were observed (Maksymiec and Krupa, 2007; Diwakar and Abdullah, 2011). Higher amount of Cu altered the concentration of photosynthetic pigments, efficiency of PSII, and organization of thylakoid membrane, and also fixation of CO2 in the plants (Patsikka et al., 2002; Liotenberg et al., 2015).

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8.2.1.2 Zinc Zinc is a trace element, which is involved in several metabolic processes in plants, including antioxidative defense, protein synthesis, the stability of genetic materials, and carbohydrate metabolism (Hall and Williams, 2003; Broadley et al., 2007; Clemens, 2006). Zinc is also a necessary element in auxin synthesis pathway (Alloway, 2004; Brennan, 2005). In addition, Zn influences the carbonic anhydrase and hydrogenase activity and participates in cytochrome synthesis and helps in stabilizing ribosomal fractions (Tisdale et al., 1984). Hafeez et al. (2013) found that Zn deficiency in plants results in abnormalities, such as stunted growth, smaller leaves, chlorosis, decreased number of tillers, spikelet sterility, and increasing crop maturity period, as well as causes harm to harvested agricultural products. Zn deficiency also increases plant’s vulnerability to different stresses such as temperature, high light, and different biotic infections (Marschner, 1995; Cakmak, 2000). Natural soil contains Zn; however, its concentration is rising due to anthropogenic activities. Zinc is mostly added to the environment through various industries and also through agricultural processes such as liquid manure, fertilizers, and pesticides (Bhagure and Mirgane, 2011). Due to this contamination of soil, Zn level frequently exceeds the requirement as nutrients and thus causes phytotoxicity (Bonnet et al., 2000; Ali et al., 2000). In the polluted soils, Zn concentration has been measured in the range of 0.15 0.3 g/kg (Devries et al., 2002). The high level of Zn in soil inhibits several metabolic processes of plants, which result in a significant decrease in plant growth and induce senescence. The first symptom to present itself in most species exhibiting chlorosis in young leaves due to Zn toxicity induced iron or manganese deficiency (Sivasankar et al., 2012); with prolonged exposure, the chlorosis may spread to older leaves in plants (Ebbs and Kochian, 1997) and results into the conversion from green to purplish-red color due to phosphorus deficiency (Yadav, 2010). Excess of Zn in plants reduced the growth, nutrient content, and photosynthetic energy conversion (Bonnet et al., 2000; Baran, 2013) and resulted in a significant decrease in the uptake of other nutrients and activities of different enzymes (Ouariti et al., 1997; Kaya et al., 2000; Khudsar et al., 2004). Zn toxicity results in the necrosis and wilting of old leaves; it also causes abnormalities in cell growth and elongation (Cakmak, 2000; Khudsar et al., 2004; Di Baccio et al., 2005). It has been previously reported that Zn can play a significant role in the restriction of stomatal conductance and therefore it may influence CO2 fixation in plants (Khudsar et al., 2004; Dhir et al., 2008; Sagardoy et al., 2010). The Zn in high concentration may also negatively influence the plant pigment levels, such as Chl a and Chl b, as well as their ratio (Cherif et al., 2010; Ivanov et al., 2012). Furthermore, excess of Zn may result in excessive reactive oxygen species (ROS), such as superoxide anion radical (O2 2 ) and hydrogen peroxide (H2O2), which influence antioxidant defense mechanism and photosynthesis in plants (Weckx and Clijsters, 1997; Cakmak, 2000; Madhava Rao and Sresty, 2000; Lopez-Millan et al., 2005). 8.2.1.3 Iron Fe is required by the plants for its metabolism and development. In general, Although, Fe is present in high concentrations in terrestrial environment, O2 rich environment generates its oxidized (ferric) form that limits its bioavailability at neutral pH (Zuo and Zhang, 2011; Samaranayake et al., 2012). Being a part of structural proteins in different important

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enzymes, plants require Fe for several important metabolic processes. Fe is having a structural role in enzymes related to the prosthetic group (including catalase, peroxidase, cytochrome oxidase, and other cytochromes) whereas it is also a part of nonheme proteins such as ferredoxin and superoxide dismutase (Marschner, 1995; Rout and Sahoo, 2015). Fe is also needed in chlorophyll synthesis, maintaining the structure of chloroplasts, regulation of respiration, photosynthesis, reduction of nitrates and sulfates, etc. (Mamatha, 2007; Ziaeian and Malakouti, 2006; Incesu et al., 2015). In soils that are rich in molecular oxygen, Fe is frequently found in its oxidized form, primarily as a component of highly insoluble oxyhydroxide polymers. Thus Fe is not adequately available in highly aerobic soil, which leads to its deficiency in the plants (known as iron chlorosis). Because of Fe involvement in chlorophyll formation, Eskandari (2011) found that deficiency of Fe leads to a visible symptom in young leaves with an appearance of pale yellow or white color in the area between leaf veins, also known as interveinal chlorosis. Further, Fe has been reported to be present in glutamyl-tRNA reductase and required for its activity in the synthesis of 5-aminolevulinic acid thus indirectly playing an important role in chlorophyll synthesis (Kumar and Soll, 2000). The solubility of Fe31 decreases with increasing pH and hence, Fe deficiency is usually observed in alkaline or overlimed soils (Briat, 2005; Schulte, 2004). Nearly one-third of the world’s cropland is highly alkaline, which is required for optimal growth of plants including staple crops such as rice (Marschner, 1995; Takahashi et al., 2001). Severe deficiency of Fe results in a high reduction of plant cell division, which results in an overall decrease in plant growth including smaller leaves (Mohamed and Aly, 2004; Manthey and Crowley, 1997). Although tightly regulated mechanism for Fe homeostasis exists in plants, its deficiency as well as overload in plant tissues is toxic. An increase in the levels of reducible Fe, an increase in K exchange, and low pH are the general characteristics of most Fetoxic soils (Parent et al., 2008). At low pH, the Fe ion is released from its oxide, which results in its availability by roots. A high level of iron is found mainly in waterlogged or flooded soils where anaerobic conditions occur. Fe31 is readily reduced under anaerobic conditions to more soluble Fe21, which has potential to enter plant cells and cause oxidative damage resulting in remarkable decline in the growth of plants (Stein et al., 2009; Zhang et al., 2011). Excess of Fe21 ions in plants may catalyze the formation of ROS especially H2O2 via the Fe-catalyzed Haber Weiss reaction (Fenton reaction), which can cause a massive amount of damage to macromolecules, such as protein, lipid, carbohydrate, and DNA, leading to cell death (Arora et al., 2002; Rastogi and Pospisil, 2012). The high concentration of Fe can cause nutrient imbalance and affect the uptake of nutrients such as P, K, Zn, Mn (Sahrawat, 2004; Baruah et al., 2007; Fageria et al., 2008). Iron toxicity is characterized by “bronzing” or “yellowing” of oldest rice leaves and formation of ROS in cells, which affects the synthesis of chlorophyll, protein, leaf free amino acid, and nitrate reductase activity. Increased uptake of Fe has been reported to reduce the protein synthesis in leaves (Baruah et al., 2007; Silveira et al., 2007; Saikia and Baruah, 2012). It has been estimated that iron toxicity may significantly reduce rice grain yield (Sahrawat, 2000; Majerus et al., 2007). To counteract Fe toxicity the plant stores Fe in its apoplast and vacuole; the antioxidant enzyme present in the plant has also been observed to increase its activity and help in detoxification of ROS forms as a result of Fe toxicity (Dufey et al., 2009; Saikia and Baruah, 2012). Ferritin is considered crucial for

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iron homeostasis. Zancani et al. (2007) found that plant ferritins were found mainly in plastids and also in mitochondria and are produced during iron congestion and photo inhibition (Murgia et al., 2002). 8.2.1.4 Manganese For most of the organisms, Mn is an essential micronutrient. Its divalent (II), trivalent (III), and tetravalent (IV) forms occur in biological systems. In soil, it exists as exchangeable Mn, Mn oxide, organic Mn, and component of Ferro-Mn silicate minerals. Amongst the various ionic species, a divalent form of Mn (Mn21) is the most soluble form found in soil, while Mn31 and Mn41 are relatively less soluble forms (Guest et al., 2002). The soil pH is known to affect the bioavailability of Mn, organic matter, moisture, soil aeration, and redox conditions (Marschner, 1995; Schulte and Kelling, 1999; Porter et al., 2004). Because of easy conversion of Mn21 to Mn31 or Mn41, Mn plays a vital role in oxidation and reduction processes in plants, such as, in electron transport chain of photosynthesis, where Mn is involved in the water-splitting process in photosynthetic machinery, whereas in mitochondria, it is present in the form of Mn-containing superoxide dismutase and helps in the scavenging of ROS (Scandalios, 1993). In the photolysis process of water, an oxygen-evolving complex associated with four Mn atoms is bound with the proteins at the reaction center of photosystem II (Goussias et al., 2002). Hence, for the oxidation of water, Mn cluster works as a catalyst (Zouni et al., 2001). As mentioned earlier, Mn is an essential component for the biosynthesis of chlorophyll, whereas it also takes part in the synthesis of tyrosine, an aromatic amino acid, and secondary metabolites such as lignin and flavonoids (Lidon et al., 2004). In addition, Mn is known to act as a cofactor for various important enzymes in plants such as phosphoenolpyruvate carboxykinase; pyruvate carboxylase; Mn-catalase, and Mn-superoxide dismutase (Burnell, 1988; Ducic and Polle, 2005). Mn is also essential for several other important metabolic processes such as ribulose bis phosphate (RuBP) carboxylase reactions; adenosine tri phosphate (ATP) synthesis; and the synthesis of proteins, acyl acids, and fatty acids (Ness and Woolhouse, 1980; Pfeffer et al., 1986; Houtz et al., 1988). Mn solubility is observed to be decreased with an increase in pH. One unit increase in pH leads to a decrease in solubility by 100 times, which makes it less available in alkaline soil, thus leading to Mn deficiency. Buchanan et al. (2000) also observed that Mn deficiency leads to impact water-splitting system in photosystem II. Thus Mn helps in providing the necessary electrons for photosynthesis. Mn absence caused leaf senescence and reduction in chlorophyll and net photosynthesis (Ahangar et al., 1995; Ndakidemi et al., 2011; Tanoi and Kobayashi, 2015). The high amount of Mn is extremely toxic and damages the plant cells (Migocka and Klobus, 2007). The quantity of Mn21 form is enhanced with a decrease in pH of the soil. The Mn21 is the form of Mn, which is taken by plants due to its solubility and negatively impacts the root growth and development (Zhao et al., 2017). Due to its high solubility, Mn21 can be easily transported through the plants by root cells and can be accumulated in plant shoot (Marschner, 1995). The Mn toxicity may cause severe damage to the basic structure in thylakoid and photosynthetic machinery, thus primarily targeting chloroplast (Lynch and St. Clair, 2004; Lidon et al., 2004; Chen et al., 2015). In plants, immoderate Mn levels altered a variety of important physiological phenomena, such as absorption,

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utilization, and translocation of other mineral elements (P, Fe, Mg, and Ca), and enzyme activity (Ducic and Polle, 2005; Lei et al., 2007). The interveinal and marginal chlorosis in leaves and necrotic leaf spots are major toxic symptoms of Mn found in several plant species (Moroni et al., 2003; Rosas et al., 2007; Mora et al., 2009). Mn toxicity also causes necrosis in the leaves of cowpea and barley (Demirevska-Kepova et al., 2004; Fuhrs et al., 2008). In rice, Mn accumulation was observed more in leaves (Lidon, 2001) while it was predominantly observed in the shoots of Sinapis alba (Farasova and Beinrohr, 1998). Thus it can be concluded that Mn is essential for plants when it is present in traces whereas very toxic when present in excess (Kochian et al., 2004; Ducic and Polle, 2005). 8.2.1.5 Nickel Nickel is a universally present trace metal that penetrates into the environment through both natural and human activities (Barrie, 1981; WHO, 1991). Ni is recognized as a necessary element for the growth and development of plant (Liu, 2001) although it is required in a very less amount for plant growth (Nieminen et al., 2007). Ni, in traces, is necessary for plants throughout all its stages in life. Furthermore, without the adequate amount of Ni, the plant will not be able to survive (Bhalerao et al., 2015). Ni is a component of nine metalloenzymes, including urease, which participates in urea hydrolysis (Takishima et al., 1988; Ragsdale, 2009). Ni is recognized to contribute in a number of key metabolic reactions such as hydrogen metabolism, ureolysis (N metabolism), methane biogenesis, and acetogenesis (Mulrooney and Hausinger, 2003). The most common form of Ni in the environment is nickelous ion (Ni21); only Ni21 is the form of Ni that is the accessible form for plants. Ni21 readily oxidizes and turns out to be unavailable at high pH. Therefore in high pH soils, the plants are susceptible to deficiency of Ni (Harasim and Filipek, 2015). In the absence of Ni the tip of the plant leaf burns, which is the result of high accumulation of urea. When in excess, Ni causes leaf chlorosis and necrosis in the plant (Mcllveen and Negusanti, 1994; Seregin and Kozhevnikova, 2006). A nickel deficiency also caused delayed nodulation and inhibited the proficiency of N fixation (Brown, 2006). The authors suggested that leguminous plants require Ni for the fixation of N. Consequently, leguminous crops, such as green bean and cowpea, needed Ni fertilization particularly in the case where Zn and Cu levels were high in the soil or if the soil was having pH higher than 6.7 (Brown, 2006). With industrialization the amount of Ni is increasing in nature. Thus it is more common to observe an excess of Ni in place of its deficiency in plants (Alloway, 1995; Salt et al., 2000). The drastic effects of higher concentration of Ni were identified at several levels, which includes molecular, physiological, and morphological changes such as a decrease in mitosis, plant growth, photosynthesis, and reduced enzymatic activity and nitrogen metabolism (Rao and Sresty, 2000; Molas, 2002; Gajewska et al., 2009; Chen et al., 2009). The excess of Ni was observed to cause hindrance in other essential metal ions’ uptake, it induced oxidative stress and produced drastic effects in fruit and crop yield (Gajewska et al., 2006; Chen et al., 2009). Extremely high Ni concentrations in the soil lead to the formation of totally inappropriate land for agricultural activity (Duarte et al., 2007). The toxic symptoms caused by high level of Ni in plants include chlorosis, necrosis, a decrease in growth of plants, and in expansion of leaves (Chen et al., 2004; Shaw et al., 2004). Ni interferes with the division and elongation of the cell (Seregin and Ivanov, 2001). It was also

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observed that Ni caused damage to the photosynthetic apparatus along with damage in tissues of epidermal and mesophyll cells (Bethkey and Drew, 1992). Excess of Ni in the plant also causes a decrease in the chlorophyll content (Gajewska and Sklodowska, 2007; Alam et al., 2007; Ahmad et al., 2007; Gajewska et al., 2006). Ni was reported to remove the Ca ions from the Ca-binding site of oxygen-evolving complex (Boisvert, 2007), whereas Ni was also reported to replace ion in chlorophyll, which ultimately leads to the reduction of electron transport chain in photosystem II (Kupper et al., 1996; Souza and Rauser, 2003). Furthermore, an excess of Ni leads to the formation of various ROS, which further damage the cells by oxidation of macromolecules (Boominathan and Doran, 2002; Hao et al., 2006). 8.2.1.6 Cobalt Co is a transition element; it has a vital role in plant growth and development (Arif et al., 2016; DalCorso et al., 2014). Weisany et al. (2013) reported that Co is essential for symbiotic association of plants with microorganisms for the fixation of nitrogen in plants. It is well established that Rhizobium and other N2-fixing microorganisms is required Co for their symbiotic association with plants. The importance of Co in N2 fixation was identified because of its involvement as a cofactor in vitamin b6 (cobalamine); it acts like a coenzyme that helps in nodule growth and N2 fixation in plants (Graham and Vance, 2000). Robson et al. (1979) reviewed the nature of the relation involving nutrient supply and combined nitrogen on growth of legumes and suggested that the Co is needed in a relatively higher amount in comparison to other nutrients for the plants where symbiotic nitrogen fixation is required for their better growth. The plants can accumulate a small amount of Co, which depends on plant species and is controlled by different metabolic processes in the plants (Li et al., 2004; Bakkaus et al., 2005). Co at low levels in soil increased the growth parameters, pigment content, biochemical and mineral content in plants (maize), while at increased level, Co negatively affects these parameters (Jaleel et al., 2009). Several studies have been previously conducted to show the toxic effects of Co in the growth and development of the plant. The high concentration of Co was observed to alter several metabolic processes inside the plant cell (Jayakumar et al., 2008; Jaleel et al., 2009; Khan and Khan, 2010; Lange et al., 2016). 8.2.1.7 Molybdenum Mo is an element, which is found in its various oxidation states ranging from zero to VI. Among them, the universal form found in majority of agricultural soil is the VI. Mo is a necessary micronutrient for plants, and molybdate is its prime form accessible to plants, which is requisite in traces and identified to contribute in the various oxidative processes of the plants (Liu et al., 2005; Kaiser et al., 2005). Mo act as a necessary part of several enzymes, which play a role in oxidative processes in plants such as nitrate reductase, aldehyde oxidase, xanthine dehydrogenase, and sulfite oxidase (Nicholas, 1975). The tomato and cauliflower plants were found to accumulate anthocyanins when grown under high concentration of Mo, which leads to the purple color of plant leaves, whereas in legumes the color of leaves was observed to be converted to yellow (Bergmann, 1992; Gupta, 1997). The reduced activity of molybdoenzymes was generally considered responsible for these phenomena in plants. The enzymes affected by Mo include the enzymes such as nitrate reductase and nitrogenase, which are considered as primary nitrogen-assimilation

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enzymes. Deficiency of Mo may appear in the form of necrotic spots on leaf lamina, and it reduces seed germination also in crop plants (Chatterjee and Nautiyal, 2001; Graham and Stangoulis, 2005). Application of lime may alleviate Mo deficiency from acid soils (Rhodes and Nangju, 1979). However, apart from essentiality of Mo; it is toxic when available in excess for the plants. The excess Mo interferes with the plant growth, yield, and quality of the seeds (Gopal et al., 2015). The production of lightweight undeveloped seeds, reduced in vigor and germination potential, was observed in both Mo deficiency and its excess (Gopal et al., 2015).

8.2.2 Toxic heavy metals 8.2.2.1 Cadmium Cd is an extremely noxious contaminant, which enters the environment through natural and human activities. Important sources of cadmium are domestic wastewater, atmospheric deposition, and industrial release (Benavides et al., 2005). Amongst all nonessential heavy metals, most attention has been given to Cd as Cd is an element that is highly toxic to human beings, and through consumption of plants and animals it can be transferred to the human. Cd also has high solubility in water, whereas it has relative high mobility in the soil plant system (Pinto et al., 2004; Hoseini and Zargari, 2013). Due to the high solubility, it can be easily absorbed through roots of plants and then relocated to the shoots (Sekara et al., 2005). Generally, the Cd toxicity was observed to be 2 20 times higher when compared with the similar concentration of other heavy metals (Shah and Dubey, 1995; De Maria et al., 2013). Cd can affect numerous morphological, physiological, and biochemical alterations in the plants (Hammami et al., 2004; Turgut et al., 2005; Azevedo et al., 2005). Cd commonly injured the roots, reduced the growth of the plants, and caused lessening of the uptake of nutrients and water (Jibril et al., 2017), stomatal conductance (Chen et al., 2011), an overall inhibition of photosynthesis (Sheoran et al., 1990), decreased the level of chlorophyll (Pandey et al., 2007), affected the assimilation of NO3 (Ali et al., 2007), and caused decrease in the yield of crops (Shah and Dubey, 1997) at higher concentrations. Cd caused oxidative stress through increasing the formation of ROS, which damaged macromolecules such as nucleic acids and proteins (Stohs et al., 2000; Schutzendubel et al., 2001). Despite the enhanced activities of antioxidants, Cd toxicity results in excess generation of malondialdehyde (MDA) production, secondary metabolites, and an increase in proline for the purpose of defending the plants against structural and physiological injuries. Jibril et al. (2017) have reported that Cd toxicity in lettuce caused an imbalance in its nutrients, resulting in the reduction of vitamin C, and as a defense mechanism resulted in the enhancement of antioxidant mechanism, increase in the level of secondary metabolites, increase in MDA production, and enhancement in proline concentration. 8.2.2.2 Lead Pb is the main environmentally distributed heavy metal in the soil. The Agency for Toxic Substances and Disease Registry has categorized it as second among all harmful substances (ATSDR, 2007). Pb is found naturally in the Earth surface from where it is released to the environment. Some anthropogenic activities also lead to the distribution of

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Pb in the environment. Pb may occur either as a free metal ion or form a complex with 22 2 inorganic components (e.g., Cl2, SO22 4 , CO3 , and HCO3 ). It can also be present as organic ligands, such as amino acids, fulvic acids, and humic acids, in soils (Uzu et al., 2009; Tabelin and Igarashi, 2009; Vega et al., 2010; Sammut et al., 2010). Srivastava et al. (2015) mentioned that human activities, such as, improper wastewater management at domestic and industrial level, the emissions from cars, batteries, paints, and treated woods may lead to Pb contamination. The use of various fertilizers in agricultural activities also contributes significantly to the release and distribution of Pb contaminant in the soil. Through the environment, Pb enters the plants and gets accumulated in different tissues; it is extremely poisonous to the existing organism, and can cause biochemical, physiological, and morphological dysfunctions in plants (Pezzarossa et al., 2011; Fahr et al.,2013). The first plant organ that comes in contact with the different components of the terrestrial water and soil is the root system (Fahr et al., 2013; Al-Akeel, 2016). Pb produced adverse effects on germination rate, root and shoot length, plant water status, seedling weight, seedling growth, vigor of seedlings, chlorophyll, nitrogen and protein contents, mineral nutrition, photosynthesis, and enzyme activities; Pb toxicity also results in chlorosis, necrosis, and senescence of the leaf (Munzuroglu and Geckil, 2002; Awan et al., 2015). Pb negatively influenced the growth of plant by decreasing the uptake and relocation of nutrients, such as Ca, Fe, Mg, P, K, Ca, Na, Zn, and Cu, in plants and by restricting the element entry to the plant cells, or coupled the ions with the carriers of ion, which makes the carrier unavailable for the uptake and relocation of other elements via roots to the leaves of the plants (Xiong, 1997; Pourrut et al., 2011; Srivastava et al., 2015). The high production of ROS due to Pb toxicity results in the oxidation of macromolecules, whereas it also triggers antioxidative mechanism (Pourrut et al., 2011). 8.2.2.3 Mercury Hg is ubiquitous, present in trace quantities throughout the lithosphere, the hydrosphere, the atmosphere, and the biosphere, as well as in igneous rocks (Goldwater, 1971). Azevedo and Rodriguez (2012) found that Hg can be converted to different oxidation states with ease. Hg is a dangerous pollutant, which can be rapidly uptaken and accumulated in plants and animals and quickly spread through its consumption in the ecosystem causing toxic effects on humans. Hg has chemical property to form various salts with amalgams (alloys), sulfur, oxygen, and chlorine, and with almost every metal, except for platinum and iron. In nature, Hg occurs both in organic and inorganic forms (e.g., methylHg). Mostly Hg2C (an inorganic form) is predominantly found in soils from where it can be easily uptaken by the plants (Chen and Yang, 2012; Gao et al., 2010; Patra and Sharma, 2000). The sediments contaminated with Hg can rapidly spread and becomes lethal to different ecosystems, including humans. Hg becomes highly toxic after its conversion into methyl mercury (Ahammad et al., 2018). The relation between Hg and plant systems is of very significant nature, which is because of its application in seed disinfectant, herbicides, and fertilizers (Cavallini et al., 1999). Recently, several studies have revealed that the products in daily use, such as cereals and vegetables, were contaminated with Hg, which was due to the presence of different Hg sources around the agriculture field. In the environment, coal-fired power plants are the prime sources of mercury (Li et al., 2017). Mostly, research work has been done on germination and morphology offshoot, root and leaf

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(Shrivastava et al., 2016). Hg has high phytotoxicity as compared to other heavy metals, and it accumulates in plant roots (Munzuroglu and Geckil, 2002; Gautam et al., 2010). Different physiological processes such as water uptake by plants, transpiration, the chlorophyll synthesis, and photosynthesis were observed to be significantly decreased after its exposure to Hg. Hg in both forms (organic/inorganic) have been found to cause loss of other elements such as Fe, Mn, Mg, and K (Boening, 2000). Hg shows a strong attraction toward sulfur, which is the cause for its toxic action in a living system, as Hg interferes with the normal functioning of several essential enzymes by binding to its sulfhydryl groups (Patra et al., 2004; Garcia and Reyes, 2001; Sharma, 1985). The inhibition of plant growth and yield production by Hg was observed in the plants due to its effect on uptake of nutrients and homeostasis, decreased chlorophyll content, increased oxidative stress, and lipid peroxidation (Sharma et al., 1990; Cho and Park, 2000; Patra and Sharma, 2000; Shiyab et al., 2009; Moreno-Jimenez et al., 2009; Ahammad et al., 2018). Hg was found to alter antioxidant defense system through the changes in the antioxidant activity of chemical agents, such as nonprotein thiols and glutathione, whereas, it also modifies the activity of antioxidant enzymes such as glutathione reductase, superoxide dismutase, and ascorbate peroxidase (Garcia and Reyes, 2001; Patra et al., 2004; Sparks, 2005; Ortega-Villasante et al., 2005; Israr et al., 2006). For removal of Hg, phytoremediation and biosorption are appropriate and successful technologies (Kumar et al., 2017). Phytoremediation is a process where the plants are having high accumulating capacity for toxic compounds, such as Hg, and thus can extract the compound from the site and then dispose the plant in such a way that the toxic compounds are converted to its inorganic form or accumulated and disposed at one place (Ahammad et al., 2018). 8.2.2.4 Chromium Cr belongs to transition metal group and a non essential element for plants. Cr occurs in various corrosion conditions, but the stable types in biological systems are Cr(III) and Cr(VI) species, whereas in the biological system, the other Cr states are moreover shortlived or unstable. Cr(III) is comparatively less movable than the element discussed earlier, which is the reason of its less contaminating nature. It is generally found bound with different organic matter in soil or water bodies, whereas Cr(VI) is highly soluble in water, moveable, and most toxic to living organisms with severe effects on humans, animals, plants, and microorganisms (Cervantes et al., 2001; Vasylkiv et al., 2010; Sangwan et al., 2014). Cr(Vi) is generally found to be combined with oxygen-like chromate (CrO22 4 ) or dichromate (Cr2 O22 ) oxyanions (Liu et al., 2015). In plants, Cr has been found to accumu7 late mainly in roots than in shoots (Lopez-Luna et al., 2009; Rahmaty and Khara, 2011). Their high concentration has been found to decrease the germination of seeds and the development of seedling (Gangaiah et al., 2013; Stambulska et al., 2018), dry matter accumulation (Vajpayee et al., 2001), and photosynthesis (Zeid, 2001). Cr was also observed to affect the translocation of different elements, such as Cu, Zn, Mn, S, and P, from roots to different parts in shoots of Mn, Cu, Zn, P, and S via roots to leaves (Chatterjee and Chatterjee, 2000). Chlorophyll content was found to decrease by various Cr compounds (Sharma and Sharma, 1996). Cr(VI) was found to inhibit CO2 absorption and photosynthesis, respiration, and symbiotic nitrogen fixation (Subrahmanyam, 2008; Singh et al., 2013). Cr in different forms may cause damage to symbiotically associated plants such as

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legumes. The plant toxicity to Cr can be again correlated with its capacity to enhance ROS formation, therefore causing the oxidation of macromolecules, which leads to activation of different antioxidant systems, such as peroxidase, guaiacol peroxidase, superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX), as a protective mechanism (Rahmaty and Khara, 2011; Stambulska et al., 2018). The production of nodule bacterial strains, which have very high resistance to Cr, can be used in the bioremediation process of Cr-contaminated area (Stambulska et al., 2018).

8.3 Water-deficit stress in plants Water-deficit stress is an abiotic constraint and a widespread threat around the world (Soltani et al., 2006). The influencing factors in water deficit are insufficient precipitation, the extreme intensity of the terrestrial salt, and the rising use of freshwater by industries. Due to all of these, water accessibility is limited for agricultural communities, especially in warm and dry areas (Porudad and Beg, 2003; Neumann, 2008). Water-deficit conditions in plants can be induced artificially to assess its effects in plants. For this, the best known selective agents are polyethylene glycol (PEG), sucrose, mannitol, or sorbitol, as they all increase the osmotic pressure in media and induce water deficit in plants (Rai et al., 2011). However, the most discriminating agent used to stimulate water stress is the high molecular weight PEG. PEG is a water-soluble polymer, nontoxic, nonmetabolized, and nonabsorbed by the cells and is accessible in a broad range of molecular weights (e.g., PEG-4000, 6000, 8000, 10,000) (Hassan et al., 2004; Lawlor, 1970). To create osmotic stress, exposure of plants with large molecular weight PEG (e.g., PEG-6000) is more suitable than smaller molecular weight, such as in PEG-4000, since germination percentage of seed in PEG-6000 and in soil is with the same water potential (Emmerich and Hardgree, 1990). In the natural environment, plants encountered water-deficit conditions at different stages of their life, and the condition altered metabolic machinery of the plant that in turn affects the plant growth.

8.3.1 Growth attributes of plants affected by water deficit The seed germination is a very critical stage of any plant life cycle. It starts with water uptake by a dry seed through imbibitions and finishes with the emergence of radicle from the seed (Welbaum et al., 1998). When a seed absorbs water, several hydrolytic enzymes get activated and start metabolizing the stored food (Raven et al., 2005). Therefore germination of the seeds is mainly an important phase of plants that demand water and is greatly influenced by water deficit. Once the seed has germinated, the root is the first organ that is exposed to water deficit. Therefore it is assumed that under water-deficit conditions, osmotic alterations in the root caused the increase in turgor pressure for constant root growth and assimilation of water and nutrients. Water-deficit stress decreased the percentage of germination, root length, and water content of the seedling and decreased the activity of the enzymes associated with the germination process. The activities of α-amylase and α-glucosidase were severely affected by osmotic stress

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(Muscolo et al., 2014). Further, water deficit affects leaf area, stem elongation, and root propagation, troubles a plant’s water relations, and decreases water-use efficiency. Moreover, the limitation of leaf growth is among the earliest visible impacts of water stress. Other visible symptoms of plant subjected to water deficit are leaf wilting, stunted plant height, the reduction in leaf area and number, and a hindrance in the development of buds and flowers (Bhatt and Srinivasa Rao, 2005). PEG-6000 induces low water potential represented by a linear decrease in both root and shoot growth, where the effect is more prominent on shoot. The process results in an improved ratio of root/shoot with an increase in stress factor. Water deficit stress reduced the dry weight of root, dry matter accumulation of leaf, leaf expansion and specific leaf area, however, enhanced leaf to root mass, leaf area to root mass ratio represent less distribution of dry matter into storage organs (Stagnari et al., 2018). In addition, water-deficit stress affects the crop physiology and biosynthesis of secondary metabolites such as, phenols, flavanoid, and induces the buildup of a large quantity of these components along with plant yield reduction (Klunklin and Savage, 2017; Ghodke et al., 2018).

8.3.2 Photosynthetic performance under water deficit Chlorophyll is an integral part of the chloroplast apparatus, which is an essential component of photosynthesis and is sensitive to water deficiency in the plant (Rahdari et al., 2012). Severe water-deficit stress was observed to cause a significant decrease in plant chlorophyll level (Mafakheri et al., 2010). A reduction in total chlorophyll content due to less availability of water may result in the low capacity for light harvesting by the plant, which is a characteristic sign of pigment photooxidation and chlorophyll deprivation (Anjum et al., 2011). Water deficit was also observed to cause changes in the ratio of chlorophyll a/b and carotenoids (Farooq et al., 2009). Generally, concentration of chlorophyll a decreases with an increase in water deficit, while chlorophyll b slightly increases under higher water deficit, which is due to an increase in protein synthesis and nitrogen metabolism. Jain et al. (2013) have reported a high reduction in chlorophyll a level than chlorophyll b. These authors also observed a substantial decrease in chlorophyll synthesis due to a significant reduction in aminolevulinic acid content and aminolevulinic-acid deaminase activity without any alteration in activity of chlorophyllase with the supply of PEG, which suggested that water deficit caused changes in the chlorophyll synthesis rather than its degradation. However, Ashraf et al. (1994) found that water stress reduced the concentration of chlorophyll b more than chlorophyll a. In the process of photosynthesis, chlorophyll is the molecule, which absorbs light with the help of accessory pigments present in the protein chlorophyll complex. The trapped light migrates toward the reactive centers of photosystem I and II, where the electron transportation takes place, resulting in the formation of nicotinamide adenine dinucleotide phosphate (reduced) (NADPH) and ATP (Horton et al., 1996). Plants grown under water-deficient conditions were observed to have a significant decrease in their stomatal conductance, which consequently serves to conserve water and tries to maintain a sufficient leaf-water status. As a consequence, a significant reduction in CO2 absorption and photosynthesis was observed in affected plants (Chaves et al., 2002). Water stress at first reduces photosynthetic activity by declining leaf area and photosynthetic rate per unit leaf area (Basu et al., 2016). Water deficit

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decreased the CO2 assimilation rates, gas exchange, and maximal carboxylation efficiency and increased the CO2 compensation point and also caused changes in the shape of CO2 curves of photosynthesis (Zlatev and Yordanov, 2004). The main effect of water scarcity is restraining photosynthesis through stomatal closure, which reduces CO2 uptake by leaves and prevents the transpirational water loss (Yokota et al., 2002; Anjum et al., 2003). Water deficit suppresses photochemical efficiency of photosystem II, which is due to a reduction in electron transport and impairment of photosynthetic machinery (Barta et al., 2010; Zlatev and Lidon, 2012). Severe drought conditions were previously reported to cause significant impairment of photosynthesis, which occurs due to the damage to RuBisCO enzyme (Bota et al., 2004). Water deficit also caused a reduction in both RuBisCO carboxylation activity and RuBP regeneration capacity. It may be suggested that RuBP regeneration can be restricted due to a decrease in the supply from light-reaction products (NADPH and ATP) or due to a decrease in the activity of other (except RuBisCO) Calvin cycle enzymes (Baker et al., 1997; Nogues and Baker, 2000).

8.3.3 Antioxidative defense mechanism under water-deficit stress Water deficiency in plant aggravates the generation of ROS, which results in oxidation of macromolecules and lipid peroxidation (Sairam et al., 2005). H2O2 and OH• are the major components, which are formed as a response to water scarcity, as observed in young bean plants (Zlatev et al., 2005). H2O2 is a strong oxidant produced as a result of  O22 scavenging. The high level of H2O2 results in the injury to cells, which cause oxidative damage, lipid peroxidation, disruption of metabolic functions, and loss of cellular integrity at its accumulation sites (Velikova et al., 2000). Organized antioxidant machinery (consisting of several enzymes as well as chemical compounds) is present in chloroplasts that prevent ROS accumulation, thus helping in the prevention of excessive damage caused due to oxidation of macromolecules (Srivalli et al., 2003). Haider et al. (2018) found an increase in the activity of MDA with an increase in the activities of antioxidative enzymes at both biochemical and molecular levels under water-deficit conditions. Under water-stress conditions the changes in the activities of SOD, APX, glutathione reductase, and CAT have a significant role in antioxidative defense mechanism (Kavas et al., 2013; Shi et al., 2014). These enzymes help in deactivation of ROS by converting it to stable form (Zhang et al., 2011). An increase in the SOD and CAT activities and a reduction in ROS, such as O2 2 and H2O2, were observed in the roots of bud seedlings of tomato (Cha-um et al., 2013). It is also suggested that increased activity of CAT induced by deficient water may remove the O2 2 and their product H2O2 (Sairam et al., 2000). Shi et al. (2014) suggested that under water-deficit stress, the exogenous supplementation of silicon may result in an increase in seed germination and improve the antioxidant defense mechanism in the tomato plants.

8.3.4 Role of osmotic adjustment and accumulation of solutes tolerant to dehydration Responses to water deficit may occur within a few seconds or in minutes and hours, which depends on the set of response mechanisms involved, and therefore, improvement

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of water-deficit tolerance is difficult. The osmotic adjustment may take part in different functions related to tolerance mechanism of water deficit (Turner, 1986; Ludlow and Muchow, 1990). The osmotic adjustment is the accumulation process of solutes by maintaining turgor in tissues in response to water-deficit stress. The process enormously depends on the photosynthesis to supply compatible solutes. Photosynthesis is inhibited under dehydration, which is related to the reduced supply of solutes for osmotic adjustment. Water deficit generally results in the reduction of water potential of leaf and a decrease in leaf area (Wullschleger et al., 2005; Farooq et al., 2009; Luo et al., 2016). It reduces leaf extension to get a balance between the water status of plant tissues and the water taken up by roots (Lonbani and Arzani, 2011). Complete loss of free water resulted in desiccation or dehydration. Therefore a small leaf area is advantageous to avoid this situation under water-deficient condition (Blum, 2005). Moreover, the high relative water content is a resistant mechanism against water scarcity and is related to more osmotic regulation or lesser elasticity of the cell wall of tissues (Ritchie et al., 1990). Accumulation of solutes help in osmotic regulation in plants, which includes organic acids, free amino acids, inorganic cations, and carbohydrates. Potassium is the primary inorganic cation in some plants, and in leaf, it is the most abundant solute that accumulates during water deficit (Ford and Wilson, 1981). Dehydrins and osmotin are proteins, which have been reported to be accumulated by several plants (such as tobacco, tomato, and maize) under water-stress condition (Ramagopal, 1993). Accumulation of solutes with a role in plantdefense mechanisms, such as proline and soluble sugar, was reported to be a unique response to various environmental stresses including water deficit (Sakamoto and Murata, 2002). The accumulation of proline in a plant was reported and considered to be the first response of plants under stress for the purpose of reducing any cellular injury (Ghorbanli et al., 2012). Increased proline content with reduced relative water content has been observed with the supply of PEG (Jain et al., 2013). Haider et al. (2018) suggested that the accumulation of components, such as proline and sorbitol, can perform as water-deficit tolerance indicators for early selection of peach cultivars under controlled conditions. Other elements that accumulated under water-stress conditions include alcohols and glycine betaine (Galston and Sawhney, 1990; Chopra and Sinha, 1998). The accumulation of abscisic acid (ABA) hormone was observed to have a significant role in response to dehydration. The use of silicon fertilizer provides a theoretical basis for avoidance of water stress in the irrigation of tomato in arid or semiarid regions (Zlatev and Lidon, 2012). Understanding these responses to water deficit is essential for screening the tolerant genotypes to water-limited conditions. Moreover, following the molecular and biochemical reactions to drought is necessary for the understanding of plant-resistance mechanisms under water-deficient conditions (Sourour et al., 2017).

8.4 Combination of metal with water-deficit stress In the natural environment, plants encountered multiple stresses simultaneously, and a combined impact of several abiotic and biotic stresses significantly limits the yield of plants. Pandey et al. (2017) categorized different biotic and abiotic stresses in three different categories- single, multiple individual and combined; where a single stress indicates

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only one individual stress factor at a time is interfering with the plant, where as, the multiple individual stress represents the impact of two or more stresses occurring at different time periods without any overlap. The occurrence of water deficiency and heavy-metal stress in the field condition at the same time is an example of combined abiotic stress (Swapna and Rama Gopal, 2014), whereas fungal pathogen and bacteria infecting a plant during the same time interval indicate a combined biotic stress (Pandey et al., 2017). In the recent past, it has been shown that a plant has a unique response against different abioticstress combinations that were not compared with the response of plants to individual stress factors (Mittler, 2006). Furthermore, the concurrent incidence of diverse stresses caused the complex plant responses that are regulated by diverse and contrasting signaling pathways (Suzuki et al., 2014). Therefore it is required to understand the plant mechanism behind the multiple and concurrent stresses, as it may help in the development of different transgenic crops and plants with improved tolerance for natural environmental conditions (Mittler, 2006; Atkinson and Urwin, 2012).

8.4.1 The combined impact of metal and water deficit on plant growth and physiological processes In natural environmental condition, different stresses coexist, thus combined stresses are real threats to the plants (Rizhsky et al., 2004; Mittler, 2006; Suzuki et al., 2014; Ramegowda and Senthil-kumar, 2015). Recent evidence showed that plants are reacting differently to multiple stresses together in comparison to their reaction toward individual stress factors (Atkinson and Urwin, 2012). Understanding the responses of plants to diverse stresses together is extremely complicated as it causes several modifications at cellular and physiological levels. According to Pandey et al. (2015), plants exhibit common responses that are common to individual stresses and combinations of stress. Ramegowda and Senthil-Kumar (2015) suggested that along with several common responses, plants revealed modified molecular and physiological responses as part of their stress tolerance approach under combined stresses. When plants are subjected to combined metal and water-deficit stress, their responses are different and sometimes unique than that of stresses when given separately. In sorghum (Sorghum bicolor L. Moench), individual application of aluminum (Al) and PEG-induced water deficit, in an increasing manner, leads to a decrease in different morphological characters such as leaf area, root length, and dry weight of root and shoot. Among these two stresses, water-deficit stress caused more severe effects on growth than Al toxicity. Zaifnejadi et al. (1997) found that by combining these two stresses, all these growth parameters were decreased. With individual Al treatment, no increase in proline content in shoots and roots was observed, but when grown with water deficit, an extensive increase in proline was observed to be higher in shoots when compared with roots. Disantea et al. (2011) observed the effects of Zn along with drought in Quercus suber L. seedlings, where the seedlings were treated first with Zn and then to severe drought for a short time. They suggested that morphological and physiological responses to Zn exposure may result in water conservation strategies by plant and alleviation of the short drought stress, but it may be not effective when plants are exposed to drought for a long term.

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Seedlings received higher doses of Zn, which leads to a higher concentration of Zn in leaves and roots with increased Zn availability and caused a decrease in rate of photosynthesis, photochemical efficiency, and specific root length. Thus it is reported that under severe drought and high concentration of Zn, the water content of detached leaves decreases to 52% whereas with low concentration of Zn, the water level remains higher than 70% (Disantea et al., 2011). Thus, in long term, Zn may have a synergistic relation with water stress that exaggerates the drought-stress effects on the plants (Disantea et al., 2011). In seedlings of black gram (Vigna mungo L.), metal stress (Cd, Cr) and PEGinduced water stress caused significant inhibitory effect on germination and early seedling growth in both single and combination of metal and water-deficit stresses (Swapna and Rama Gopal, 2015). Early seedling growth phase was more sensitive than germination phase in combined treatments (Swapna and Rama Gopal, 2015). Water stress and heavy metals both caused reduction in seedling growth in green gram (Vigna radiata L.) as the seed germination percentage and shoot and root length reduced considerably with increased concentration of metals (Cd, Cr) and PEG-induced water deficit. Cd caused more damage than Cr and Cd also results in higher toxic impact on root growth when compared with shoot growth. Interactive effects between heavy metal and water stress on dry weight and root length was also found significant, though the interactive effect of both stresses were less than additive (Swapna and Rama Gopal, 2014). Krizek et al. (2008) found that chloroplasts were most sensitive to combination of metal and waterdeficit stress. A combined treatment of plants with high concentration of Al and high drought on Al-sensitive cultivar “Romania HS-52” of sunflower (Helianthus annuus L.) results in smaller chloroplasts and less starch in chloroplasts when compared with cv. Manchurian (Al-tolerant cultivar) (Krizek et al., 2008). The small size of chloroplasts may mean a smaller amount of grana stacks per unit area when compared with the grana stacks from the tolerant plant. Al-sensitive cultivars were observed to be more tolerant to drought than Al-tolerant cultivars. An increase in the moisture level in soil was observed to reduce Al toxicity in Al-sensitive cultivars, and likewise, a decrease in Al stress results in less damage due to high water-deficit stress (Krizek et al., 2008). Antioxidant defense mechanism is one of the key pathways, which help plants tolerate combined stress. Several studies have established the relationship of high antioxidant capacity or a decrease in ROS concentration for resistance against the combination of the stresses (Sales et al., 2013). In pigeon pea seedlings, lipid peroxidation and activities of different antioxidative enzymes, such as, polyphenol oxidase, superoxide dismutase, ascorbate peroxidase, glutathione reductase and catalase, were higher in both root and shoots under individual stress of Cd, Cr and PEG-induced water deficit. Both water stress and heavy metals increased the ROS generation and caused oxidative stress, whereas the combination of PEG treatment with Cd triggered more stress than the combination with Cr. Among all the treatments, water stress was observed to cause more damage when compared with the heavy-metal stress, whereas the combined effect was less than additive (Battana and Ghanta, 2014). Moreover, evidences from different researches suggested that plants respond to a particular combination of stresses in a nonadditive manner, producing effects that are different than the study of individual stress (Mittler, 2006). Therefore it is important to consider the combination of stresses as a new stress factor (Mittler, 2006).

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8.4.2 Plant water relations under metal stress In response to heavy-metal stress, the plants, at the initial stage, show a disturbance in their water balance. It is proposed that metal, when combined with the soil, results in poor water-holding capacity, which leads to the water-deficit stress. Therefore it is most likely that the heavy metal and water-deficit stress is faced by the plant at the same time (Derome and Nieminen, 1998). As discussed earlier the metal ions may cause root inhibition, reduction in enzymatic activity, oxidative damage to membranes, and may result in a significant decrease in photosynthesis (Hartley et al., 1999; Shaw et al., 2004). The poor health condition of plant may influence the response toward additional stress, such as water deficit, and may result in smaller root system with blocked aquaporins as well as a significant decrease in water-use efficiency (Yang et al., 2004; Ionenko et al., 2006; Ryser and Emerson, 2007). Aquaporins function as narrow protein pores, which facilitate passive movement of water molecules. Ionenko et al. (2006) have suggested that heavy metal Hg is an efficient blocker of most aquaporins and acts as a water channel inhibitor, affects intracellular osmotic equilibration, and the regulation of transcellular water transport. Using Allium cepa epidermal cells as a model system, it was demonstrated that heavy metals, such as He, Pb, Cd, and Zn, can change the conductivity of aquaporin, which leads to a significant reduction in the cell-membrane permeability for water (PrzedpelskaWasowicz and Wierzbicka, 2011). Drought along with different heavy metals (Ni, Cu, Co, and Cr) was observed to negatively impact the red maple growth by causing the alteration in its xylem structure and thus interfering with the plant’s hydraulic conductivity (De Silva et al., 2012). In Acer saccharinum L. seedlings, Cd exposure was observed to reduce the relative conductivity of excised stem sections significantly. The observed reduction may be either due to decreased xylem tissue, or due to a decrease in the size of xylem vessels, the partial blockage of xylem elements might have played a role too (Lamoreaux and Chaney, 1977). Moreover, heavy metals influence the water uptake by roots, as in roots, metals affect the factors that regulate water entry. This results in the slowdown of shortdistance water movements in different plant parts, such as symplast and apoplast, which in turn significantly decrease the flow of water in the vascular tissues of plants thus impacting the water supply to the shoot (Rucinska-Sobkowiak, 2016). It may be assumed that a decrease in transmembrane water transfer may be related to the reduction in waterchannel permeability (Rucinska-Sobkowiak et al., 2013). Furthermore, it has been observed that due to the inhibition of transpiration, the heavy metals affect water supply to the shoot, which results in a decrease of the leaf size, the thickness of the lamina, and reduced intercellular spaces, which impact the stomatal size and density (Rucinska-Sobkowiak, 2016). Metal-induced water deficit was observed to cause a significant increase in the stomata number, which is not because of an increase in stomata formation but which can be related to a decrease in guard-cell sizes under metal stress (Wainwright and Woolhouse, 1977; Neelu Kumar et al., 2000). A study in Atriplex atacamensis shows the accumulation of arsenic (As) and its distribution in plants (Vromman et al., 2011). The authors observed that the young seedlings of plant close its stomata to avoid water stress. The study on Lolium perenne indicates that under Cr stress, a significant difference in osmotic potential in plant leaves appeared when compared with control. The study suggests that the

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changes in osmotic potential may be partly because of osmotic alteration (Vernay et al., 2007). Metals may induce the storage of osmotically active solutes in plants, which may help in water uptake (Gadallah, 2000). Besides, heavy metals may reduce the plant size, which leads to the feedback mechanism, due to which a relative increase in water and nutrients was observed (Santala and Ryser, 2009). Water potential of split root system was decreased by PEG-induced water deficit in Solanum nigrum, a heavy metal accumulator plant that strongly influences root activities and hence plant’s phytoremediation capacity (Feller et al., 2015). The unavailability of the research work and information related to the combined effects of drought and heavy metals on plants are shocking as the occurrence of these stresses together in the environment is very common (IPCC, 2001; Penuelas and Filella, 2002).

8.5 Conclusions and future perspective

Stress combinations

In environmental conditions, crops and other plants are facing different biotic and abiotic stresses together, which interact with plants in various ways to give differential responses (Fig. 8.1). The combination of heavy metal and water-deficit stress is one of the examples of abiotic-stress combinations. In addition to the individual heavy metal and water-deficit effects on plants (Fig. 8.2), a combination of both the stresses affects plant growth and yield parameters in a manner that is way different from that of individual stresses. Moreover, researches have suggested that water deficit might also be provoked by heavy-metal stress. Therefore it is needed to observe the interaction of these two abiotic

Interaction

Effects on plant

References

Additive

Aggravates effects of one of the stresses

de Silva et al. (2012)

Makes the plants less susceptible to one of the stresses

Swapna and Rama Gopal (2014)

Works together to give enhanced or cumulative results

Cherif et al. (2011)

Less than additive

Synergistic

Negative

Affects crop yield and productivity

Prasad (2011) Vile (2012)

Positive

Has some beneficial effects on plants

Low et al. (2013)

FIGURE 8.1 Abiotic stress interactions and their effects on plants.

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8.5 Conclusions and future perspective

193

Water deficit stress

Metal stress

• Reduced seed germination and seedling growth

• Dehydration, decreased seed germination and seedling growth

• Stunted growth

• Osmotic imbalance

• Anatomical alterations

• Changes in anatomy and morphology

• Decreased nutrient uptake

• Reduction in cell size

• Chloroplast disorganization, decreased photosynthesis, and decreased chlorophyll

• Stomatal closure

• Changes in enzymatic activities related to photosynthesis • Inhibition of electron-transport chain

• Decrease in photosynthesis and crop productivity • Generation of reactive oxygen species and increased activities of antioxidative enzymes

• Generation of reactive oxygen species

FIGURE 8.2 Effects of metal and water deficit stress on plants.

stresses with plants for better understanding of the net impact of their combinations on plants. Researchers in the laboratory are extensively studying different abiotic-stress factors affecting the plant growth in the field in an individual manner. But the studies on combined effects of metal and water-deficit stress are restricted to very few reports. Besides, our awareness of the biochemical and molecular mechanisms that manage the response of plants to the combinations of these two stresses, are also inadequate in the available literature. Therefore extensive research is essential to decipher these mechanisms. Evaluations of multiple stresses are also very significant to get a practical view of the impact of dynamic environmental conditions. The studies have shown that combined stress leads to a further decrease in plant growth when compared with individual stress, which suggests the urgency behind such research for the purpose of developing more resistant crops. The combination of different stresses can be handled as a novel type of stress to observe different defense and acclimation responses. Consequently, the plant improvement with better adaptation under field needs to be focused toward understanding the reactions of the plant under combined stress conditions.

Acknowledgments Financial support by UGC fellowship for PhD (F1-17.1/2015-16/RGNF) to Mamta Hirve and Department of Science Technology Women Scientists-A Scheme (SR/WOS-A/LS-17/2017-G) to Dr. Sunita Kataria is thankfully acknowledged.

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References Abdelrahman, M., Burritt, M.J., Tran, L.S.P., 2017. The use of metabolomic quantitative trait locus mapping and osmotic adjustment traits for the improvement of crop yields under environmental stresses. Sem. Cell Dev. Biol. 16, 4 9. Agarwal, S., Grover, A., 2006. Molecular biology, biotechnology and genomics of flooding-associated low O2 stress response in plants. Crit. Rev. Plant Sci. 25, 1 21. Ahammad, S.J., Sumithra, S., Senthilkumar, P., 2018. Mercury uptake and translocation by indigenous plants. Rasayan J. Chem. 11, 1 12. Ahangar, A.G., Karimian, A., Assad, M., Emam, Y., 1995. Growth and manganese uptake by soybean in highly calcareous soil as affected by native and applied manganese and predicted by nine different extractants. J. Plant Nutr. 17, 117 125. Ahmad, M.S.A., Hussain, M., Saddiq, R., Alvi, A.K., 2007. Mungbean: a nickel indicator, accumulator or excluder? Bull. Environ. Contam. Toxicol. 78, 319 324. Al-Akeel, K., 2016. Lead uptake, accumulation and effects on plant growth of common reed (Phragmites australis (Cav.) Trin. ex Steudel) plants in hydroponic culture. Int. J. Adv. Agric. Environ. Eng. 3, 2. Alam, M.M., Hayat, S., Ali, B., Ahmad, A., 2007. Effect of 28-homobrassinolide treatment on nickel toxicity in Brassica juncea. Photosynthetica 45, 139 142. Ali, G., Srivastava, P.S., Iqbal, M., 2000. Influence of cadmium and zinc on growth and photosynthesis of Bacopa monnieri cultivated in vitro. Biol. Plant. 43, 599 601. Ali, B., Rani, I., Hayat, S., Ahmad, A., 2007. Effect of 4-Cl-indole-3-acetic acid on the seed germination of Cicer arietinum exposed to cadmium. Acta Bot. Croat. 66, 57 65. Alloway, B.J., 1995. In heavy metal in soilsIn: Alloway, B.J. (Ed.), second ed. Blackie Academic and Professional, London, pp. 25 34. Alloway, B.J., 2004. In Zinc in Soil and Crop Nutrition. International Zinc Association, Brussels, Belgium. Anjum, F., Yaseen, M., Rasul, E., Wahid, A., Anjum, S., 2003. Water stress in barley (Hordeum vulgare L.). I. Effect on chemical composition and chlorophyll contents. Pak. J. Agric. Sci. 40, 45 49. Anjum, S., Xie, X., Wang, L., Saleem, M., Man, C., Lei, W., 2011. Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agric. Res. 6, 2026 2032. Arif, N., Yadav, V., Singh, S., Singh, S., Ahmad, P., Mishra, R.K., et al., 2016. Influence of high and low levels of plant beneficial heavy metal ions on plant growth and development. Front. Environ. Sci. 4, 69. Arora, A., Sairam, R.K., Srivastava, G.C., 2002. Oxidative stress and antioxidative system in plants. Curr. Sci. 82, 1227 1338. Ashraf, M.Y., Azmi, A.R., Khan, A.H., Ala, S.A., 1994. Effect of water stress on total phenols, peroxidase activity and chlorophyll content in wheat. Acta Physiol. Plant. 16, 185 191. Atkinson, N.J., Urwin, P.E., 2012. The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 63, 3523 3544. ATSDR, 2007. Priority List of Hazardous Substances. Agency for Toxic Substances and Diseases Registry. Available from: ,http://www.atsdr.cdc.gov/. (accessed 28.07.09.). Awan, S., Jabeen, M., Imran, Q.M., Ullah, F., Mehmood, Z., Jahngir, M., et al., 2015. Effects of lead toxicity on plant growth and biochemical attributes of different rice (Oryza sativa L.) varieties. J. Bio-Mol. Sci. 3, 44 55. Azevedo, R., Rodriguez, E., 2012. Phytotoxicity of mercury in plants: a review. J. Bot. 1 6. Article ID 848614. Azevedo, H., Pinto, C.G.G., Fernandes, J., Loureiro, S., Santos, C., 2005. Cadmium effects on sunflower growth and photosynthesis. J. Plant Nutr. 28, 2211 2220. Baker, N.R., Nogues, S., Allen, D.J., 1997. Photosynthesis and photoinhibition. In: Lumsden, P.J. (Ed.), Plants and UV-B: Responses to Environmental Change. Cambridge University Press, Cambridge, pp. 95 111. Bakkaus, E., Gouget, B., Gallien, J.P., Khodja, H., Carrot, H., Morel, J.L., et al., 2005. Concentration and distribution of cobalt in higher plants: the use of micro-PIXE spectroscopy. Nucl. Inst. Methods B 231, 350 356. Baran, A., 2013. Assessment of Zea mays sensitivity to toxic content of zinc in soil. Pol. J. Environ. Stud. 22, 77 83. Barrie, L.A., 1981. Atmospheric nickel in Canada, Effects of Nickel in the Canadian Environment, 3. National Research Council of Canada No. 18568, pp. 55 76. Barta, C., Dunkle, A.M., Wachter, R.M., Salvucci, M.E., 2010. Structural changes associated with the acute thermal instability of Rubisco activase. Arch Biochem. Biophys. 499, 17 25.

Plant Life under Changing Environment

References

195

Baruah, K.K., Das, S., Das, K., 2007. Physiological disorder of rice associated with high levels of iron in growth medium. J. Plant Nutr. 30, 1871 1883. Basu, S., Ramegowda, V., Kumar, A., Pereira, A., 2016. Plant adaptation to drought stress. F1000Research 5, 1554. F100 Faculty Rev. Battana, S., Ghanta, R.G., 2014. Antioxidative enzyme responses under single and combined effect of water and heavy metal stress in two Pigeon pea cultivars. J Sci. Innov. Res. 3, 72 80. Benavides, M.P., Susana, M., Tomaro, M., 2005. Cadmium toxicity in plants. Braz. J. Plant Physiol. 17, 21 34. Bergmann, W., 1992. Nutritional disorders of plants. Visual and Analytical Diagnosis. Gustav Fischer Verlag, Jena. Bethkey, P.C., Drew, M.C., 1992. Stomatal and non-stomatal components to inhibition of photosynthesis in leaves of Capsicum annuum during progressive exposure to NaCl salinity. Plant Physiol. 99, 219 226. Bhagure, G.R., Mirgane, S.R., 2011. Heavy metal concentrations in ground waters and soils of Thane Region of Maharashtra, India. Environ. Monit. Assess. 173, 643 652. Bhalerao, S.A., Sharma, A.S., Poojari, A.C., 2015. Toxicity of nickel in plants. Int. J. Pure Appl. Biosci. 3, 345 355. Bhatt, R.M., Srinivasa Rao, N.K., 2005. Influence of pod load response of okra to water stress. Indian J. Plant Physiol. 10, 54 59. Blum, A., 2005. Mitigation of Drought Stress by Crop Management. Available from: ,www.PlantStress.com.. Boening, D.W., 2000. Ecological effects, transport, and fate of mercury: a general review. Chemosphere 40, 1335 1351. Boisvert, S., 2007. Inhibition of the oxygen-evolving complex of photosystem II and depletion of extrinsic polypeptides by nickel. Biometals 20, 879 889. Bonnet, M., Camares, O., Veisseire, P., 2000. Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo). J Exp. Bot. 51, 945 953. Boominathan, R., Doran, P.M., 2002. Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. New Phytol. 156, 205 215. Bota, J., Medrano, H., Flexas, J., 2004. Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytol. 162, 671 681. Brennan, R.F., 2005. Zinc Application and Its Availability to Plants. Ph.D. dissertation). School of Environmental Science, Division of Science and Engineering, Murdoch University. Briat, J.F., 2005. Iron from soil to plant products. Bull. Acad. Natl. Med. 189, 1609 1619. Broadley, M.R., White, P.J., Hammond, J.P., Zelko, I., Lux, A., 2007. Zinc in plants. New Phytol. 173, 677 702. Brown, P.H., 2006. Nickel. In: Barker, A.V., Pilbeam, D.J. (Eds.), Handbook of Plant Nutrition. CRC Press Taylor & Francis Group, Boca Raton, FL, pp. 395 410. Buchanan, B., Grusen, W., Jones, R., 2000. Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Maryland, 1367 p. Burnell, J., 1988. The biochemistry of manganese in plants. In: Graham, R.D., Hannam, R.J., Uren, N.J. (Eds.), Manganese in Soil and Plants. Kluwer Academic Publishers, Dordrecht, The Netherlands, 125 137pp. Caglieri, A., Goldoni, M., Acampa, O., Andreoli, R., Vettori, M.V., et al., 2006. The effect of inhaled chromium on different exhaled breath condensate biomarkers among chrome-plating workers. Environ. Health Perspect. 114, 542 546. Cakmak, I., 2000. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 146, 185 205. Cavallini, A., Natali, L., Durante, M., Maserti, B., 1999. Mercury uptake, distribution and DNA affinity in durum wheat (Triticum durum Desf.) plants. Sci. Total Environ. 243 244, 119 127. Cervantes, C., Campos-Garcıa, J., Devars, S., et al., 2001. Interactions of chromium with microorganisms and plants. FEMS Microbiol. Rev. 25, 335 347. Chatterjee, C., Nautiyal, N., 2001. Molybdenum stress affects viability and vigour of wheat seeds. J. Plant Nutr. 24, 1377 1386. Chatterjee, J., Chatterjee, C., 2000. Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ. Pollut. 109, 69 74.

Plant Life under Changing Environment

196

8. Heavy metals, water deficit, and their interaction in plants: an overview

Cha-um, S., Samphumphuang, T., Kirdmanee, C., 2013. Glycinebetaine alleviates water deficit stress in Indica rice using proline accumulation, photosynthetic efficiencies, growth performances and yield attributes. AJCS 7, 213 218. Chaves, M.M., Pereira, J.S., Maroco, J., Rodrigues, M.L., Ricardo, C.P.P., Osorio, M.L., et al., 2002. How plants cope with water stress in the field. Photosynthesis and growth. Ann. Bot. 89, 907 916. Chen, J., Yang, Z.M., 2012. Mercury toxicity, molecular response and tolerance in higher plants. Biol. Met. 25, 847 857. Chen, C., Chen, T.H., Lo, K.F., Chiu, C.Y., 2004. Effects of proline on copper transport in rice seedlings under excess copper stress. Plant Sci. 166, 103 111. Chen, C., Huang, D., Liu, J., 2009. Functions and toxicity of nickel in plants: recent advances and future prospects. Clean 37, 304 313. Chen, X., Wang, J., Shi, Y., Zhao, M.Q., Chi, G.Y., 2011. Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Bot. Stud. 52, 41 46. Chen, Z., Sun, L., Liu, P., Liu, G., Tian, J., Liao, H., 2015. Malate synthesis and secretion mediated by a Mn enhanced malate dehydrogenase, SgMDH1, confers superior Mn tolerance in Stylosanthes guianensis. Plant Physiol. 167, 176 188. Cherif, J., Derbel, N., Nakkach, M., von Bergmann, H., Jemal, F., Ben Lakhdar, Z., 2010. Analysis of in vivo chlorophyll fluorescence spectra to monitor physiological state of tomato plants growing under zinc stress. J. Photochem. Photobiol. B. 101, 332 339. Cho, U.H., Park, J.O., 2000. Mercury-induced oxidative stress in tomato seedlings. Plant Sci. 156, 1 9. Chopra, R.K., Sinha, S.K., 1998. Prospects of success of biotechnological approaches for improving tolerance to drought stress in crop plants. Curr. Sci. 74, 25 34. Clemens, S., 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88, 1707 1719. DalCorso, G., Manara, A., Piasentin, S., Furini, A., 2014. Nutrient metal elements in plants. Metallomics 6, 1770 1788. De Maria, S., Puschenreiter, M., Rivelli, A.R., 2013. Cadmium accumulation and physiological response of sunflower plants to Cd during the vegetative growing cycle. Plant Soil Environ. 59, 254 261. De Silva, N.D.G., Cholewa, E., Ryser, P., 2012. Effects of combined drought and heavy metal stresses on xylem structure and hydraulic conductivity in red maple (Acer rubrum L.). J. Exp. Bot. 63, 5957 5966. Demirevska, K., Zasheva, D., Dimitrov, R., Simova-Stoilova, L., Stamenova, M., Feller, U., 2009. Drought stress effects on Rubisco in wheat: changes in the Rubisco large subunit. Acta Physiol. Plant. 31, 1129 1138. Demirevska-kepova, K., Simova-Stoilova, L., Stoyanova, Z., Holzer, R., Feller, U., 2004. Biochemical changes in barely plants after excessive supply of copper and manganese. Environ. Exp. Bot. 52, 253 266. Derome, J., Nieminen, T., 1998. Metal and macronutrient fluxes in heavy-metal polluted Scots pine ecosystems in SW Finland. Environ. Pollut. 103, 219 228. Devries, W., Lofts, S., Tipping, E., Meili, M., Groenenberg, J.E., Schutze, G., 2002. Impact of soil properties on critical concentrations of cadmium, lead, copper, zinc and mercury in soil and soil solution in view of ecotoxicological effects. Rev. Environ. Contam. Toxicol. 191, 47 89. Dhir, B., Sharmila, P., Pardha Sarad, P., 2008. Photosynthetic performance of Salvinia natans exposed to chromium and zinc rich wastewater. Braz. J. Plant Physiol. 20, 61 70. Di Baccio, D., Kopriva, S., Sebastiani, L., Rennenberg, H., 2005. Does glutathione metabolism have a role in the defense of poplar against zinc excess? New Phytol. 167, 73 80. Disantea, K.B., Fuentesb, D., Cortinaa, J., 2011. Response to drought of Zn-stressed Quercus suber L. seedlings. Environ. Exp. Bot. 70, 96 103. Diwakar, G., Abdullah, 2011. Toxicity of copper and cadmium on germination and seedling growth of maize (Zea maize L.) seeds. Indian J. Sci. Res. 2, 67 70. Duarte, B., Delgado, M., Ca-ador, I., 2007. The role of citric acid in cadmium and nickel uptake and translocation, in Halimione portulacoides. Chemosphere 69, 836 840. Ducic, T., Polle, A., 2005. Transport and detoxification of manganese and copper in plants. Braz. J. Plant Physiol. 17, 103 112. Dufey, I., Hakizimana, P., Draye, X., Lutts, S., Bertin, P., 2009. QTL mapping for biomass and physiological parameters linked to resistance mechanisms to ferrous iron toxicity in rice. Euphytica 167, 143 160.

Plant Life under Changing Environment

References

197

Ebbs, S.D., Kochian, L.V., 1997. Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J. Environ. Qual. 26, 776 781. Emamverdian, A., Ding, Y., Mokhberdoran, F., Xie, Y., 2015. Heavy metal stress and some mechanisms of plant defense responses. Sci. World J. 756120, 18 p. Emmerich, W.E., Hardgree, S.P., 1990. Poly ethylene glycol solution contact effects on seed germination. Agron. J. 82, 1103 1107. Eskandari, H., 2011. The importance of iron (Fe) in plant products and mechanism of its uptake by plants. J. Appl. Environ. Biol. Sci. 1, 448 452. Fageria, N.K., Santos, A.B., Filho, M.P., Guimaries, C.M., 2008. Iron toxicity in lowland rice. J. Plant Nutr. 31, 1676 1697. Fahr, M., Laplaze, L., Bendao, N., Hocher, V., El Mzibri, M., Bogusz, D., et al., 2013. Effect of lead on root growth. Front. Plant Sci. 4 (175), 1 7. Farasova, A., Beinrohr, E., 1998. Metal-metal interaction in accumulation of V, Ni, Mo, Mn, and Cu in under and above ground parts of Sinapis alba. Chemosphere 36, 1305 1317. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S.M.A., 2009. Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29, 185 212. Feller, U., Anders, I., Wei, S., 2015. Effects of PEG-induced water deficit in Solanum nigrum on Zn and Ni uptake and translocation in split root systems. Plants 4, 284 297. Ford, C.W., Wilson, J.R., 1981. Changes in levels of solutes during osmotic adjustment to water stress in leaves of four tropical pasture species. Aust. J. Plant Physiol. 8, 77 91. Fuhrs, H., Hartwig, M., Buitrago, L., Heintz, D., Van Dorsselaer, A., Braun, H., et al., 2008. Early manganesetoxicity response in Vigna unguiculata L. a proteomic and transcriptomic study. Proteomics 8, 149 159. Gadallah, M.A.A., 2000. Effects of indole-3-acetic acid and zinc on the growth, osmotic potential and soluble carbon and nitrogen components of soybean plants growing under water deficit. J. Arid Environ. 44, 451 467. Gajewska, E., Sklodowska, M., 2007. Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20, 27 36. Gajewska, E., Sklodowska, M., Slaba, M., Mazur, J., 2006. Effect of nickel on antioxidative enzyme activities, proline and chlorophyll content in wheat shoots. Biol. Plant. 50, 653 659. Gajewska, E., Wielanek, M., Bergier, K., Skłodowska, M., 2009. Nickel-induced depression of nitrogen assimilation in wheat roots. Acta Physiol. Plant. 3, 1291 1300. Galston, A.W., Sawhney, R.K., 1990. Polyamines in plant physiology. Plant Physiol. 94, 406 410. Gangaiah, A., Chandrasekha, R.T., Varaprasad, D., Hima Bindu, Y., Keerthi Kumari, M., Chakradhar, T., et al., 2013. Effects of heavy metals on in vitro seed germination and seedling growth of Pennisetum glacum (L.). R. Br. Int. J Food Agric. Vet. Sci. 3, 87 93. Gao, S., Yang, C.O., Tang, L., Zhu, J.Q., Xu, Y., Wang, S.H., et al., 2010. Growth and antioxidant responses in Jatropha curcas seedling exposed to mercury toxicity. J. Hazard. Mater. 182, 591 597. Garcia, E.M., Reyes, R.E., 2001. Synthesis pattern of an Hg-binding protein in Acetabularia calyculus during shortterm exposure to mercury. Bull. Environ. Contam. Toxic. 66, 357 364. Gautam, M., Sengar, R.S., Chaudhary, R., Sengar, K., Garg, S., 2010. Possible cause of inhibition of seed germination in two rice cultivars by heavy metals Pb2C and Hg2C. Toxicol. Environ. Chem. 92, 1111 1119. Ghodke, P.H., Andhale, P.S., Gijare, U.M., Thangasamy, A., Khade, Y.P., Mahajan, V., et al., 2018. Physiological and biochemical responses in onion crop to drought stress. Int. J. Curr. Microbiol. App. Sci. 7, 2054 2062. Ghorbanli, M., Gafarabad, M., Amirkian, T., Mamaghani, B.A., 2012. Investigation of proline, total protein, chlorophyll, ascorbate and dehydro-ascorbate changes under drought stress in Akria and Mobil tomato cultivars. Irish J. Plant Physiol. 3, 651 658. Goldwater, L.J., 1971. Mercury in the environment. Sci. Am. 224, 15 21. Gopal, R., Sharma, Y.K., Shukla, A.K., 2015. Effect of molybdenum stress on growth, yield and seed quality in black gram. J. Plant Nutr. 39, 463 469. Goussias, C., Boussac, A., Rutherford, W., 2002. Photosystem II and photosynthetic oxidation of water: an overview. Philos. Trans. R. Soc. Lond. B 357, 1369 1381. Graham, P.H., Vance, C.P., 2000. Nitrogen fixation in perspective, an overview of research and extension needs. Field Crops Res. 65, 93 106.

Plant Life under Changing Environment

198

8. Heavy metals, water deficit, and their interaction in plants: an overview

Graham, R.D., Stangoulis, J.R.C., 2005. Molybdenum and disease. In: Dantoff, L., Elmer, W., Huber, D. (Eds.), Mineral Nutrition and Plant Diseases. APS Press, St Paul, MN. Guest, C., Schulze, D., Thompson, I., Huber, D., 2002. Correlating manganese X-ray absorption near-edge structure spectra with extractable soil manganese. Soil Sci. Soc. Am. J. 66, 1172 1181. Gupta, U.C., 1997. Symptoms of molybdenum deficiency and toxicity in crops. In: Gupta, U.C. (Ed.), Molybdenum in Agriculture. Cambridge University Press, Cambridge. Hafeez, B., Khanif, Y.M., Saleem, M., 2013. Role of zinc in plant nutrition—a review. Am. J. Exp. Agric. 3, 374 391. Haider, M.S., Kurjogi, M.M., Khalil-ur-Rehman, M., Pervez, T., Songtao, J., Fiaz, M., et al., 2018. Drought stress revealed physiological, biochemical and gene-expressional variations in ‘Yoshihime’ peach (Prunus persica L.) cultivar. J. Plant Interact. 13, 83 90. Hall, J.L., Williams, L.E., 2003. Transition metal transporters in plants. J. Exp. Bot. 54, 2601 2613. Hammami, S.S., Chaffai, R., Ferjiani, E.E., 2004. Effect of cadmium on sunflower growth, leaf pigment and photosynthetic enzymes. Pak. J. Biol. Sci. 7, 1419 1426. Hao, F., Wang, X., Chen, J., 2006. Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci. 170, 151 158. Harasim, P., Filipek, T., 2015. Nickel in the environment. J. Elem. 20, 525 534. Hartley, J., Cairney, J.W.G., Freestone, P., Woods, C., Meharg, A.A., 1999. The effects of multiple metal contamination on ectomycorrhizal Scots pine (Pinus sylvestris) seedlings. Environ. Pollut. 106, 413 424. Hassan, N.M., Serag, M.S., El-Feky, F.M., 2004. Changes in nitrogen content and protein profiles following in vitro selection of NaCl resistant mung bean and tomato. Acta Physiol. Plant. 26, 165 175. Hawkes, J.S., 1997. Heavy metals. J. Chem. Educ. 74, 1369 1374. Hirel, B., Le Goulis, J., Ney, B., Gallais, A., 2007. The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 58, 2369 2387. Horton, P., Ruban, A., Walters, R., 1996. Regulation of light harvesting in green plants. Annu. Rev. Plant Biol. 47, 655 684. Hoseini, S.M., Zargari, F., 2013. Cadmium in plants: a review. Int. J. Farm. Allied Sci. 2, 579 581. Houtz, R.L., Nable, R.O., Cheniae, G.M., 1988. Evidence for effects on the in vivo activity of ribulose-biphosphate carboxylase/oxygenase during development of Mn toxicity in tobacco. Plant Physiol. 86, 1143 1149. Incesu, M., Yesiloglu, T., Cimen, B., Yilmaz, B., 2015. Influences of different iron levels on plant growth and photosynthesis of W. Murcott mandarin grafted on two rootstocks under high pH conditions. Turk. J. Agric. For. 39, 838 844. Ionenko, I.F., Anisimov, A.V., Karimova, F.G., 2006. Water transport in maize roots under the influence of mercuric chloride and water stress: a role of water channels. Biol. Plant. 50, 74 80. IPCC, 2001. Climate change 2001: the scientific basis. Contribution of Working Group I. In: Hougton, J.T., Dung, Y., Griggs, D.J., Noguer, M., Vander Linden, P.J., Dui, X., et al.,Third Assessment Report of Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge. Israr, M., Sahi, S., Datta, R., Sarkar, D., 2006. Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65, 591 598. Ivanov, Y.V., Savochkin, Y.V., Kuznetsov, V.V., 2012. Scots pine as a model plant for studying the mechanisms of conifers adaptation to heavy metal action: 2. Functioning of antioxidant enzymes in pine seedlings under chronic zinc action. Russ. J. Plant Physiol. 59, 50 58. Jain, M., Mittal, M., Gadre, R., 2013. Effect of PEG-6000 imposed water deficit on chlorophyll metabolism in maize leaves. J. Stress Physiol. Biochem. 9, 262 271. Jaleel, C.A., Jayakumar, K., Chang-Xing, Z., Iqbal, M., 2009. Low concentration of cobalt increases growth, biochemical constituents, mineral status and yield in Zea mays. J. Sci. Res. 1, 128 137. Jayakumar, K., Jaleel, C.A., Azooz, M.M., 2008. Impact of cobalt on germination and seedling growth of Eleusine coracana L. and Oryza sativa L. under hydroponic culture. Global J. Mol. Sci. 3, 18 20. Jibril, S.A., Hassan, S.A., Ishak, C.F., Wahab, P.E.M., 2017. Cadmium toxicity affects phytochemicals and nutrient elements composition of Lettuce (Lactuca sativa L.). Adv. Agric. 7, 1 7. Kaiser, B.N., Gridley, K.L., Brady, J.N., Phillips, T., Tyerman, S.D., 2005. The role of molybdenum in agricultural plant production. Ann. Bot. 96, 745 754.

Plant Life under Changing Environment

References

199

ˇ ca´k, M., Brestic, M., Daszkowska-Golec, A., Sitko, K., et al., 2018. Prompt chlorophyll Kalaji, H.M., Rastogi, A., Zivˇ fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica 56, 353 361. Kavas, M., Baloglu, M.C., Akca, O., Kose, F.S., Gokcay, D., 2013. Effect of drought stress on oxidative damage and antioxidant enzyme activity in melon seedlings. Turk. J. Biol. 37, 491 498. Kaya, C., Higgs, D., Burton, A., 2000. Plant growth, phosphorus nutrition and acid phosphatase enzyme activity in three tomato cultivars grown hydroponically at different zinc concentrations. J. Plant Nutr. 23, 569 579. Khan, M.R., Khan, M.M., 2010. Effect of varying concentration of nickel and cobalt on the plant growth and yield of chickpea. Aust. J. Basic Appl. Sci. 4, 1036 1046. Khudsar, T., Mahmooduzzafar, Iqbal, M., Sairam, R.K., 2004. Zinc-induced changes in morpho-physiological and biochemical parameters in Artemisia annua. Biol. Plant. 48, 255 260. Klunklin, W., Savage, G., 2017. Effect on quality characteristics of tomatoes grown under well-watered and drought stress conditions. Foods 6, 56. Kochian, L., Hoekenga, O., Pineros, M., 2004. How do crops plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu. Rev. Plant Biol. 55, 459 493. Krizek, D.T., Foy, C.D., Wergin, W.P., 2008. Role of water stress in differential aluminum tolerance of six sunflower cultivars grown in an acid soil. J. Plant Nutr. 11, 387 408. Kumar, A.M., Soll, D., 2000. Antisense HEMA1 RNA expression inhibits heme and chlorophyll biosynthesis in Arabidopsis. Plant Physiol. 122, 49 56. Kumar, B., Smita, K., Flores, L.C., 2017. Plant mediated detoxification of mercury and lead. Arabian J. Chem. 10, S2335 S2342. Kupper, H., Kupper, F., Spiller, M., 1996. Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. J. Exp. Bot. 47, 259 266. Lamoreaux, R.J., Chaney, W.R., 1977. Growth and water movement in silver maple seedlings affected by cadmium. J. Environ. Qual. 6, 201 205. Lange, B., van der Ent, A., John, A., Baker, M., Echevarria, G., Gregory Mahy, G., et al., 2016. Copper and cobalt accumulation in plants: a critical assessment of the assessment of the current state of knowledge. New Phytol. 213, 537 551. Lasat, M.M., 2002. Phytoextraction of toxic metals. A review of biological mechanism. J. Environ. Qual. 31, 109 120. Lei, Y., Korpelainen, H., Li, C., 2007. Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68, 686 694. Li, Z., McLaren, R.G., Metherell, A.K., 2004. The availability of native and applied soil cobalt to ryegrass in relation to soil cobalt and manganese status and other soil properties. N. Z. J. Agric. Res. 47, 33 43. Li, R., Wu, H., Ding, J., Fu, W., Gan, L., Li, Y., 2017. Mercury pollution in vegetables, grains and soils from areas surrounding coal-fired power plants. Sci. Rep. 7, 46545. Lidon, F., 2001. Tolerance of rice to excess manganese in the early stages of vegetative growth. Characterization of manganese accumulation. J. Plant Physiol. 158, 1341 1348. Lidon, F.C., Barreiro, M., Ramalho, J., 2004. Manganese accumulation in rice: implications for photosynthetic functioning. J. Plant Physiol. 161, 1235 1244. Liotenberg, S., Steunou, A.S., Durand, A., Bourbon, M.L., Bollivar, D., Hansson, M., et al., 2015. Oxygendependent copper toxicity: targets in the chlorophyll biosynthesis pathway identified in the copper efflux ATPase CopA deficient mutant. Environ. Microbiol. 17, 1963 1976. Liu, G.D., 2001. A new essential mineral element nickel. Plant Nutr. Fert. Sci. 7, 101 103. Liu, P., Yang, Y.S., Xu, G.D., Fang, Y.H., Yang, Y.A., Kalin, R.M., 2005. The effect of molybdenum and boron in soil on the growth and photosynthesis of three soybean varieties. Plant Soil Environ. 51, 197 205. Liu, J., Sun, Z., Lavoie, M., Fan, X., Bai, X., Qian, H., 2015. Ammonium reduces chromium toxicity in the fresh water alga Chlorella vulgaris. Appl. Microbiol. Biotechnol. 99, 3249 3258. Lawlor, D.W., 1970. Absorption of polyethylene glycols by plants and their effects on plant growth. New Phytol. 69, 501 514. Lonbani, M., Arzani, A., 2011. Morpho-physiological traits associated with terminal drought stress tolerance in triticale and wheat. Agric. Res. 9, 315 329.

Plant Life under Changing Environment

200

8. Heavy metals, water deficit, and their interaction in plants: an overview

Lopez-Luna, J., Gonzalez-Chavez, M.C., Esparza-Garcıa, F.J., Rodrıguez-Vazquez, R., 2009. Toxicity assessment of soil amended with tannery sludge, trivalent chromium and hexavalent chromium, using wheat, oat and sorghum plants. J. Hazard. Mater. 163, 829 834. Lopez-Millan, A.F., Ellis, D.R., Grusak, M.A., 2005. Effect of zinc and manganese supply on the activities of superoxide dismutase and carbonic anhydrase in Medicago truncatula wild type and raz mutant plants. Plant Sci. 168, 1015 1022. Ludlow, M.M., Muchow, R.C., 1990. A critical evaluation of traits for improving crop yields in water-limited environment. Adv. Agron. 43, 107 153. Luo, H.H., Zhang, Y.L., Zhang, W.F., 2016. Effect of water stress and rewatering on photosynthesis, root activity, and yield of cotton with drip irrigation under mulch. Photosynthetica 54, 65 73. Lynch, J.P., St. Clair, S.B., 2004. Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crop. Res. 90, 101 115. Madhava Rao, K.V., Sresty, T.V.S., 2000. Antioxidative parameters in the seedlings of pigeon-pea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci. 157, 113 128. Mafakheri, A., Siosemardeh, A., Bahramnejad, B., Struik, P.C., Sohrabi, Y., 2010. Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Aust. J. Crop Sci. 4, 580 585. Majerus, V., Bertin, P., Swenden, V., Fortemps, A., Lobre´aux, S., Lutts, S., 2007. Organ-dependent responses of the African rice to short-term iron toxicity: ferritin regulation and antioxidative responses. Biol. Plant. 51, 303 312. Maksymiec, W., Krupa, Z., 2007. Effects of methyl jasmonate and excess copper on root and leaf growth. Biol. Plant. 51, 322 326. Mamatha, N., 2007. Effect of Sulphur and Micronutrients (Iron and Zinc) on Yield and Quality of Cotton in a Vertisol (M.S. thesis). Department of Soil Science and Agricultural Chemistry College of Agriculture, Dharwad University of Agricultural Sciences, Dharwad-580 005. Manthey, J.A., Crowley, D.E., 1997. Leaf and root responses to iron deficiency in avocado. J. Plant Nutr. 20, 683 693. Marschner, H., 1995. Mineral Nutrition of Higher Plants, second ed. Academic Press, London. Martinez-Penalver, A., Grana, E., Reigosa, M.J., Sanchez-Moreiras, A.M., 2012. The early response of Arabidopsis thaliana to cadmium- and copper-induced stress. Environ. Exp. Bot. 78, 1 9. Mcllveen, W.D., Negusanti, J.J., 1994. Nickel in the terrestrial environment. Sci. Total Environ. 148, 109 138. Migocka, M., Klobus, G., 2007. The properties of the Mn, Ni and Pb transport operating at plasma membranes of cucumber roots. Physiol. Plant. 129, 578 587. Mittler, R., 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15 19. Mohamed, A.A., Aly, A.A., 2004. Iron deficiency stimulated some enzymes activity, lipid peroxidation and free radicals production in Borago officinalis induced in vitro. Int. J. Agric. Biol. 6, 179 184. Molas, J., 2002. Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni II complexes. Environ. Exp. Bot. 47, 115 126. Monni, S., Salemma, M., Millar, N., 2000. The tolerance of Empetrum nigrum to copper and nickel. Environ. Pollut. 109, 221 229. Mora, M., Rosas, A., Ribera, A., Rengel, R., 2009. Differential tolerance to Mn toxicity in perennial ryegrass genotypes: involvement of antioxidative enzymes and root exudation of carboxylates. Plant Soil 320, 79 89. Moreno-Jimenez, E., Esteban, E., Carpena-Ruiz, R., Pealosa, J., 2009. Arsenic-and mercury-induced phytotoxicity in the Mediterranean shrubs Pistacia lentiscus and Tamarix gallica grown in hydroponic culture. Ecotoxicol. Environ. Saf. 72, 1781 1789. Moroni, J., Scott, B., Wratten, N., 2003. Differential tolerance of high manganese among rapseed genotypes. Plant Soil 253, 507 519. Mulrooney, S.B., Hausinger, R.P., 2003. Nickel uptake and utilization by microorganisms. FEMS Microbiol. Rev. 27, 239 261. Munzuroglu, O., Geckil, H., 2002. Effects of metals on seed germination, root elongation, and coleoptile and hypocotyls growth in Triticum aestivum and Cucumis sativus. Arch. Environ. Contamin. Toxicol. 43, 203 213. Murgia, I., Delledonne, M., Soave, C., 2002. Nitric oxide mediates iron-induced ferritin accumulation in Arabidopsis. Plant J. 30, 521 528.

Plant Life under Changing Environment

References

201

Muscolo, A., Sidari, M., Anastasi, U., Santonoceto, C., Maggio, A., 2014. Effect of PEG-induced drought stress on seed germination of four lentil genotypes. J. Plant Int. 9, 354 363. Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8, 199 216. Nakashima, K., Yamaguchi-Shinozaki, K., 2006. Regulons involved in osmotic stress-responsive and cold stressresponsive gene expression in plants. Physiol. Plant. 126, 62 71. Ndakidemi, P.A., Bambara, S.J., Makoi, H.J.R., 2011. Micronutrient uptake in common bean (Phaseolus vulgaris L.) as affected by Rhizobium inoculation, and the supply of molybdenum and lime. Plant Omics: J. Plant Biol. Omics 4, 40 52. Neelu Kumar, M., Tomar, M., Bhatnagar, A.K., 2000. Influence of cadmium on growth and development of Vicia faba Linn. Indian J. Exp. Biol. 38, 819 823. Ness, P.J., Woolhouse, H.W., 1980. RNA synthesis in Phaseolus chloroplasts. 1. Ribonucleic acid synthesis and senescing leaves. J. Exp. Bot. 31, 223 233. Neumann, P.M., 2008. Coping mechanisms for crop plants in drought-prone environments. Ann. Bot. 101, 901 907. Nicholas, D.J.D., 1975. The function of trace elements in plants. In: Nicholas, D.J.D., Edan, A.R. (Eds.), Trace Elements in Soil Plant Animal Systems. Academic Press, New York, pp. 181 198. Nieminen, T.M., Ukonmaanaho, L., Rausch, N., Shotyk, W., 2007. Biogeochemistry of nickel and its release into the environment. Met. Ions Life Sci. 2, 1 30. Nogues, S., Baker, N.R., 2000. Effects of drought on photosynthesis in Mediterranean plants grown under enhanced UV-B radiation. J. Exp. Bot. 51, 1309 1317. Ortega-Villasante, C., Rellan-Alvarez, R., del Campo, F.F., Carpena-Ruiz, R.O., Hernandez, L.E., 2005. Cellular damage induced by cadmium and mercury in Medicago sativa. J. Exp. Bot. 56, 2239 2251. Ouariti, O., Gouia, H., Ghorbal, M.H., 1997. Response of bean and tomato plants to cadmium: growth, mineral nutrition and nitrate reduction. Plant Physiol. Biochem. 35, 347 354. Pandey, P., Irulappan, V., Bagavathiannan, M.V., Senthil-Kumar, M., 2017. Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front. Plant Sci. 8, 537. Pandey, S., Gupta, K., Mukherjee, A.K., 2007. Impact of cadmium and lead on Catharanthus roseus a phytoremediation study. J. Environ. Biol. 28, 655 662. Pandey, P., Ramegowda, V., Senthil-Kumar, M., 2015. Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front. Plant Sci. 6, 723. Parent, C., Capelli, N., Berger, A., Crevecoeur, M., Dat, J.F., 2008. An overview of plant responses to soil waterlogging. Plant Stress 2, 20 27. Patra, M., Sharma, A., 2000. Mercury toxicity in plants. Bot. Rev. 66, 379 422. Patra, M., Bhowmik, N., Bandopadhyay, B., Sharma, A., 2004. Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ. Exp. Bot. 52, 199 223. Patsikka, E., Kairavuo, M., Sersen, F., Aro, E.M., Tyystjarvi, E., 2002. Excess copper predisposes photosystem II to photoinhibition in vivo by out competing iron and causing decrease in leaf chlorophyll. Plant Physiol. 129, 1359 1367. Penuelas, J., Filella, I., 2002. Metal pollution in Spanish terrestrial ecosystems during the twentieth century. Chemosphere 46, 501 505. Pezzarossa, B., Gorini, F., Petruzelli, G., 2011. Heavy metal and selenium distribution and bioavailability in contaminated sites: a tool for phytoremediation. In: Selenium, H.M. (Ed.), Dynamics and Bioavailability of Heavy Metals in the Root Zone. CRC Press, Boca Raton, FL, pp. 93 128. Pfeffer, P.E., Tu, S., Gerasimowicz, W.V., Cavanaugh, J.R., 1986. In vivo 31P NMR studies of corn root tissue and its uptake of toxic metals. Plant Physiol. 80, 77 84. Pilon, M., Abdel-Ghany, S.E., Cohu, C.M., Gogolin, K.A., Ye, H., 2006. Copper cofactor delivery in plant cells. Curr. Opin. Plant Biol. 9, 256 263. Pinto, A.P., Mota, A.M., Pinto, F.C., 2004. Influence of organic matter on the uptake of cadmium, zinc, copper and iron by Sorghum plants. Sci. Environ. J. 326, 239 247.

Plant Life under Changing Environment

202

8. Heavy metals, water deficit, and their interaction in plants: an overview

Porter, G., Bajita-Locke, J., Hue, N., Strand, S., 2004. Manganese solubility and phytotoxicity affected by soil moisture, oxygen levels, and green manure additions. Commun. Soil Sci. Plant. Anal. 35, 99 116. Porudad, S.S., Beg, A., 2003. Safflower: a suitable oil seed for dryland areas of Iran. In: Proceeding of Seventh International Conference on Development of Drylands. Sep. 14 17. Tehran, Iran. Pourrut, B., Shahid, M., Dumat, C., Winterton, P., Pinelli, E., 2011. Lead uptake, toxicity, and detoxification in plants. Rev. Environ. Contam. Toxic. 213, 113 136. Przedpelska-Wasowicz, E.M., Wierzbicka, M., 2011. Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. Protoplasma 248, 663 671. Ragsdale, S., 2009. Nickel-based enzyme systems. J. Biol. Chem. 284, 18571 18575. Rahdari, P., Hoseini, S.M., Tavakoli, S., 2012. The studying effect of drought stress on germination, proline, sugar, lipid, protein and chlorophyll content in Purslane (Portulaca oleracea L.) leaves. J. Med. Plants. Res. 6, 1539 1547. Rahmaty, R., Khara, J., 2011. Effects of vesicular arbuscular mycorrhiza Glomus intraradices on photosynthetic pigments, antioxidant enzymes, lipid peroxidation, and chromium accumulation in maize plants treated with chromium. Turk. J. Biol. 35, 51 58. Rai, M.K., Kalia, R.K., Singh, R., Gangola, M.P., Dhawan, A.K., 2011. Developing stress tolerant plants through in vitro selection—an overview of the recent progress. Environ. Exp. Bot. 71, 89 98. Ramagopal, S., 1993. Advances in understanding the molecular biology of drought and salinity tolerance in plants—the first decade. In: Lodha, M.L., Mehta, S.L., Ramagopal, S., Srivastava, G.P. (Eds.), Adv. Pl. Biotech. Biochem. Indian Society of Agriculture Biochemists, Kanpur, India, pp. 39 48. Ramegowda, V., Senthil-kumar, M., 2015. The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J. Plant Physiol. 176, 47 54. Rao, K.V.M., Sresty, T.V.S., 2000. Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan L.) Millspauga in response to Zn and Ni stress. Plant Sci. 157, 113 128. Rastogi, A., Pospisil, P., 2012. Production of hydrogen peroxide and hydroxyl radical in potato tuber during the necrotrophic phase of hemibiotrophic pathogen Phytophthora infestans infection. J. Photochem. Photobiol. B: Biol. 117, 202 206. Raven, P.H., Evert, R.F., Eichhorn, 2005. Biology of Plants, seventh ed. W.H. Freeman and Company Publishers, New York, 504 508 pp. Reeves, R.D., Baker, A.J.M., 2000. Metal-accumulating plants. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment., 93 . Wiley, New York, p. 229. Rhodes, E.R., Nangju, D., 1979. Effects of pelleting cowpea and soybean seed with fertilizer dusts. Exp. Agric. 15, 27 32. Ritchie, S.W., Nguyan, H.T., Holaday, A.S., 1990. Leaf water content and gas exchange parameters of two wheat genotypes differing in drought resistance. Crop Sci. 30, 105 111. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S., Mittler, R., 2004. When defense pathway scollide. The response of Arabidopsisto a combination of drought and heat stress. Plant Physiol. 134, 1683 1696. Robson, A.D., Dilworth, M.J., Chatel, D.L., 1979. Cobalt and nitrogen fixation in Lupinus angustifolius L. I. Growth, nitrogen concentrations and cobalt distribution. New Phytol. 83, 53 62. Rosas, A., Rengel, Z., Mora, M., 2007. Manganese supply and pH influence growth, carboxylate exudation and peroxidase activity of ryegrass and white clover. J. Plant Nutr. 30, 253 270. Rout, G.R., Sahoo, S., 2015. Role of iron in plant growth and metabolism. Rev. Agric. Sci. 3, 1 24. Rucinska-Sobkowiak, R., 2016. Water relations in plants subjected to heavy metal stresses. Acta Physiol. Plant. 38, 257. Rucinska-Sobkowiak, R., Nowaczyk, G., Krzesłowska, M., Rabe˛da, I., Jurga, S., 2013. Water status and water diffusion transport in lupine roots exposed to lead. Environ. Exp. Bot. 87, 100 109. Ryser, P., Emerson, P., 2007. Growth, root and leaf structure, and biomass allocation in Leucanthemum vulgare Lam. (Asteraceae) as influenced by heavy-metal containing slag. Plant Soil 59, 2461 2467. Sagardoy, R., Vazquez, S., Florez-Sarasa, I.D., Albacete, A., Ribas-Carbo, M., Flexas, J., et al., 2010. Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytol. 187, 145 158. Sahrawat, K.L., 2000. Elemental composition of the rice plant as affected by iron toxicity under field conditions. Commun. Soil Sci. Plant Anal. 31, 2819 2827.

Plant Life under Changing Environment

References

203

Sahrawat, K.L., 2004. Iron toxicity in wetland rice and role of other nutrients. J. Plant Nutr. 27, 1471 1504. Saikia, T., Baruah, K.K., 2012. Iron toxicity tolerance in rice (Oryza sativa) and its association with anti-oxidative enzyme activities. J. Crop Sci. 3, 90 94. Sairam, R.K., Srivastava, G.C., Saxena, D.C., 2000. Increased antioxidant activity under elevated temperature; a mechanism of heat stress tolerance in wheat genotypes. Biol. Plant. 43, 245 251. Sairam, R., Srivastava, G., Agarwal, S., Meena, R.C., 2005. Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biol. Plant. 49, 85 91. Sakamoto, A., Murata, N., 2002. The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 25, 163 171. Sales, C.R., Ribeiro, R.V., Silveira, J.A., Machado, E.C., Martins, M.O., Lagoa, A.M., 2013. Superoxide dismutase and ascorbate peroxidase improve the recovery of photosynthesis in sugarcane plants subjected to water deficit and low substrate temperature. Plant Physiol. Biochem. 73, 326 336. Salt, D.E., et al., 2000. In: Terry, N., Banuelos, G. (Eds.), Phytoremediation of Contaminated Soil and Water. Lewis Publishers, Boca Raton, FL, 189 200pp. Samaranayake, P., Peiris, B.D., Dssanayake, S., 2012. Effect of excessive ferrous (Fe21) on growth and iron content in rice (Oryza sativa). Int. J. Agric. Biol. 14, 296 298. Sammut, M., Noack, Y., Rose, J., Hazemann, J., Proux, O., Depoux Ziebel, M., et al., 2010. Speciation of Cd and Pb in dust emitted from sinter plant. Chemosphere 78, 445 450. Sangwan, P., Kumar, V., Joshi, U.N., 2014. Effect of chromium(VI) toxicity on enzymes of nitrogen metabolism in cluster bean (Cyamopsis tetragonoloba L.). Enzyme Res. 1 9. Article ID 784036. Santala, K.R., Ryser, P., 2009. Influence of heavy-metal contamination on plant response to water availability in white birch, Betula papyrifera. Environ. Exp. Bot. 66, 334 340. Scandalios, J., 1993. Oxygen stress and superoxide dismutases. Plant Physiol. 101, 7 12. Schulte, E.E., 2004. Soil and applied iron. Understanding Plant Nutr., A. 35 54. Schulte, E.E., Kelling, K.A., 1999. Soil and applied manganese. Understanding Plant Nutr. A2526. Schutzendubel, A., Schwanz, P., Teichmann, T., et al., 2001. Cadmium induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol. 127, 887 898. Sekara, A., Poniedziaek, M., Ciura, J., Jedrszczyk, E., 2005. Cadmium and lead accumulation and distribution in the organs of nine crops: implications for phytoremediation. Pol. J. Environ. Stud. 14, 509 516. Seregin, I.V., Ivanov, V.B., 2001. Physiological aspects of cadmium and lead toxic effects on higher plants. Russ. J. Plant Physiol. 48, 523 544. Seregin, I.V., Kozhevnikova, A.D., 2006. Physiological role of nickel and its toxic effects on higher plants. Russ. J. Plant Physiol. 53, 257 277. Shah, K., Dubey, S., 1995. Effect of cadmium on RNA level as well as activity and forms of Ribonuclease in growing rice seedlings. Plant Physiol. J. 33, 577 584. Shah, K., Dubey, R.S., 1997. Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biol. Plant. 40, 121 130. Sharma, S.S., 1985. Effect of mercury on germination and seedling growth, mobilization of food reserves and activity of hydrolytic enzymes in Pisum sativum. Environ. Exp. Bot. 25, 189 193. Sharma, D.C., Sharma, C.P., 1996. Chromium uptake and toxicity effects on growth and metabolic activities in wheat, Triticum aestivum L. cv. UP 2003. Indian J. Exp. Biol. 34, 689 691. Sharma, A., Talukder, G., Sharma, A., 1990. Advances in Cell and Chromosome Research. Aspect Publications Ltd, West Yorkshire, pp. 197 213. Shaw, B.P., Sahu, S.K., Mishra, R.K., 2004. Heavy metal induced oxidative damage in terrestrial plants. In: Prasad, M. (Ed.), Heavy Metal Stress in Plants from Biomolecules to Ecosystems, second ed Springer-Verlag, New York. Sheoran, I.S., Signal, H.R., Singh, R., 1990. Effect of cadmium and nickel on photosynthesis and the enzymes of photosynthetic carbon reduction cycle in pigeon pea (Cajanus cajan L.). Photosynth. Res. 23, 345 351. Shi, Y., Zhang, Y., Yao, H., Wu, J., Sun, H., Gong, H., 2014. Silicon improves seed germination and alleviates oxidative stress of bud seedlings in tomato under water deficit stress. Plant Physiol. Biochem. 78, 27 36. Shiyab, S., Chen, J., Han, F.X., Monts, D.L., Matta, F.B., Gu, M., et al., 2009. Mercury-induced oxidative stress in Indian mustard (Brassica juncea L.). Environ. Toxicol. 24, 462 471.

Plant Life under Changing Environment

204

8. Heavy metals, water deficit, and their interaction in plants: an overview

Shrivastava, S., Shrivastava, A., Sharma, J., 2016. Detoxification mechanisms of mercury toxicity in plants: a review. Recent Adv. Biol. Med. 1, 60 68. Silveira, V.C., Oliveira, A.P., Sperotto, R.A., Espindola, L.S., Amaral, L., Dias, J.F., et al., 2007. Influence of iron on mineral status of two rice (Oryza sativa L.) cultivars. Braz. J. Plant Physiol. 19, 127 139. Singh, H.P., Mahajan, P., Kaur, S., Batish, D.R., Kohli, R.K., 2013. Chromium toxicity and tolerance in plants. Environ. Chem. Lett. 11, 229 254. Sivasankar, R., Kalaikandhan, R., Vijayarengan, P., 2012. Phytoremediating capability and nutrient status of four plant species under zinc stress. Int. J. Res. Plant Sci. 2, 8 15. Soltani, A., Gholipoor, M., Zeinali, E., 2006. Seed reserve utilization and seedling growth of wheat as affected by drought and salinity. Environ. Exp. Bot. 55, 195 200. Sourour, A., Afef, O., Mounir, R., Mongi, B.Y., 2017. A review: morphological, physiological, biochemical and molecular plant responses to water deficit stress. Int. J. Eng. Sci. 6, 01 04. Souza, J.F., Rauser, W.E., 2003. Maize and radish sequester excess cadmium and zinc in different ways. Plant Sci. 65, 1009 1022. Sparks, D.L., 2005. Toxic metals in the environment: the role of surfaces. Elements 4, 193 197. Srivalli, B., Chinnusami, V., Renu, K.C., 2003. Antioxidant defense in response to abiotic stresses in plants. J. Plant Biol. 30, 121 139. Srivastava, D., Singh, A., Baunthiyal, M., 2015. Lead toxicity and tolerance in plants. J. Plant Sci. Res. 2, 123. Stagnari, F., Galieni, A., D’Egidio, S., Pagnani, G., Pisante, M., 2018. Responses of radish (Raphanus sativus) to drought stress. Ann. Appl. Biol. 172, 170 186. Stambulska, U.Y., Bayliak, M.M., Lushchak, V.I., 2018. Chromium(VI) toxicity in legume plants: modulation effects of rhizobial symbiosis. BioMed Res. Int. 8031213, 13p. Stein, R.J., Duarte, G.L., Spohr, M.G., Lopes, S.I.G., Fett, J.P., 2009. Distinct physiological responses of two rice cultivars subjected to iron toxicity under field conditions. Ann. Appl. Biol. 154, 269 277. Stohs, S.J., Bagchi, D., Hassoun, E., Bagchi, M., 2000. Oxidative mechanisms in the toxicity of chromium and cadmium ions. J. Environ. Pathol. Toxicol. Oncol. 19, 201 213. Subrahmanyam, D., 2008. Effects of chromium toxicity on leaf photosynthetic characteristics and oxidative changes in wheat (Triticum aestivum L.). Photosynthetica 46, 339 345. Suzuki, N., Rivero, R.M., Shulaev, V., Blumwald, E., Mittler, R., 2014. Abiotic and biotic stress combinations. New Phytol. 203, 32 43. Swapna, B., Rama Gopal, G., 2014. Interactive effects between water stress and heavy metals on seed germination and seedling growth of two green gram (Vigna radiata L. Wilzec) cultivars. Biolife 2, 291 296. Swapna, B., Rama Gopal, G., 2015. Germination and early growth responses of Vigna mungo L. Hepper cultivars to water stress and heavy metals. Am. J. Sci. Med. Res. 1 (2), 169 174. Tabelin, C., Igarashi, T., 2009. Mechanisms of arsenic and lead release from hydrothermally altered rock. J. Hazard. Mater. 169, 980 990. Takahashi, M.T., Nakanishi, H., Kawasaki, S., Nishizawa, N.K., Mori, S., 2001. Nat. Biotechnol. 19, 466. Takishima, K., Suga, T., Mamiya, G., 1988. The structure of jack bean urease. The complete amino-acid sequences, limited proteolysis and reactive cysteine residue. Eur. J. Biochem. 175, 151 165. Tanoi, K., Kobayashi, N.I., 2015. Leaf Senescence by magnesium deficiency. Plants 4, 756 772. Tisdale, S.L., Nelson, W.L., Beaten, J.D., 1984. Zinc In Soil Fertility and Fertilizers, fourth ed. Macmillan Publishing Company, New York, 382 391pp. Turgut, C., Pepe, M.K., Cutright, T.J., 2005. The effect of EDTA on Helianthus annuus uptake, selectivity and translocation of heavy metals when grown in Ohio, New Mexico and Colombia soils. Chemosphere 58, 1087 1095. Turner, N.C., 1986. Adaptation to water deficits: a changing perspective. Aust. J. Plant Physiol. 13, 175 189. Uzu, G., Sobanska, S., Aliouane, Y., Pradere, P., Dumat, C., 2009. Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation. Environ. Pollut. 157, 1178 1185. Vajpayee, P., Rai, U.N., Ali, M.B., Tripathi, R.D., Yadav, V., Sinha, S., 2001. Chromium induced physiological changes in Vallisneria spiralis L and its role in phytoremediation of tannery effluent. Bull. Environ. Contam. Toxicol. 67, 246 256.

Plant Life under Changing Environment

References

205

Vasylkiv, O.Y., Kubrak, O.I., Storey, K.B., Lushchak, V.I., 2010. Cytotoxicity of chromium ions may be connected with induction of oxidative stress. Chemosphere 80, 1044 1049. Vega, F., Andrade, M., Covelo, E., 2010. Influence of soil properties on the sorption and retention of cadmium, copper and lead, separately and together, by 20 soil horizons: comparison of linear regression and tree regression analyses. J. Hazard. Mater. 174, 522 533. Velikova, V., Yordanov, I., Edreva, A., 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Protective role of exogenous polyamines. Plant Sci. 151, 59 66. Vernay, P., Gauthier-Moussard, C., Hitmi, A., 2007. Interaction of bioaccumulation of heavy metal chromium with water relation, mineral nutrition and photosynthesis in developed leaves of Lolium perenne L. Chemosphere 68, 1563 1575. Vromman, D., Flores-Bavestrello, A., Slejkovec, Z., Lapaille, S., Teixeira-Cardoso, C., Briceno, M., et al., 2011. Arsenic accumulation and distribution in relation to young seedling growth in Atriplex atacamensis Phil. Sci. Total Environ. 412 413, 286 295. Wainwright, S.J., Woolhouse, H.W., 1977. Some physiological aspects of copper and zinc tolerance in Agrostis tenuis sibth.: cell elongation and membrane damage. J. Exp. Bot. 28, 1029 1036. Weckx, J.E.J., Clijsters, H.M.M., 1997. Zn phytotoxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiol. Biochem. 35, 405 410. Weisany, W., Raei, Y., Allahverdipoor, K.H., 2013. Role of some of mineral nutrients in biological nitrogen fixation. Bull. Environ. Pharmacol. Life Sci. 2, 77 84. Welbaum, G.E., Bradford, K.J., Kyu-Ock, Y., Oluoch, M.O., 1998. Biophysical, physiological and biochemical processes regulating seed germination. Seed Sci. Res. 8, 161 172. World Health Organization (WHO), 1991. Nickel: Environmental Health Criteria, 108. World Health Organization, Geneva. Wullschleger, S., Loewith, R., Oppliger, W., Hall, M.N., 2005. Molecular organization of target of rapamycin complex 2. J. Biol. Chem. 280, 30697 30704. Xiong, Z.T., 1997. Bioaccumulation and physiological effects of excess lead in a roadside pioneer species Sonchus oleraceus L. Environ. Pollut. 97, 275 279. Yadav, S.K., 2010. Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South Afr. J. Bot. 76, 167 179. Yang, H.M., Zhang, X.Y., Wang, G.X., 2004. Effects of heavy metals on stomatal movements in broad bean leaves. Russ. J. Plant Physiol. 51, 464 468. Yokota, A., Kawasaki, S., Iwano, M., Nakamura, C., Miyake, C., Akashi, K., 2002. Citrulline and DRIP-1 protein (ArgE Homologue) in drought tolerance of wild watermelon. Ann. Bot. 89, 825 832. Zaifnejadi, M., Clarki, R.B., Sullivan, C.Y., 1997. Aluminum and water stress effects on growth and proline of sorghum. J. Plant Physiol. 150, 338 344. Zancani, M., Peresson, C., Tubaro, F., Vianello, A., Macri, F., 2007. Mitochondrial ferritin distribution among plant organs and its involvement in ascorbate mediated iron uptake and release. Plant Sci. 173, 182 189. Zeid, I.M., 2001. Responses of Phaseolus vulgaris to chromium and cobalt treatments. Biol. Plant. 44, 111 115. Zhang, Y., Zhang, G.H., Liu, P., Song, J.M., Xu, G.D., Cai, M.Z., 2011. Morphological and Physiological responses of root tip cells to Fe21 toxicity in rice. Acta Physiol. Plant. 33, 683 689. Zhao, J., Wang, W., Zhou, H., Wang, R., Zhang, P., Wang, H., et al., 2017. Manganese toxicity inhibited root growth by disrupting auxin biosynthesis and transport in Arabidopsis. Front. Plant Sci. 8, 272. Ziaeian, A.H., Malakouti, M.J., 2006. Effects of Fe, Mn, Zn and Cu fertilization on the yield and grain quality of wheat in the calcareous soils of Iran. Plant Nutr. Food Sec. Sustain. Agroecosyst. 92, 840 841. Zlatev, Z., Lidon, F.C., 2012. An overview on drought induced changes in plant growth, water relations and photosynthesis. Emirates J. Food Agric. 24, 57 72. Zlatev, Z., Yordanov, I., 2004. Effects of soil drought on photosynthesis and chlorophyll fluorescence in common bean plants. Bulg. J. Plant Physiol. 30, 3 18. Zlatev, Z., Lidon, F.C., Ramalho, J.C., Yordanov, I.T., 2005. Comparison of resistance to drought of three bean cultivars. Biol. Plant. 50, 389 394.

Plant Life under Changing Environment

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8. Heavy metals, water deficit, and their interaction in plants: an overview

Zouni, A., Witt, H., Kern, J., Fromme, P., Kraub, N., Saenger, W., et al., 2001. Crystal structure of photosystem II ˚ resolution. Nature 409, 739 743. from Synechococcus elongatus at 3.8 A Zuo, Y., Zhang, F., 2011. Soil and crop management strategies to prevent iron deficiency in crops. Plant Soil 339, 83 95.

Further reading Van Assche, F., Clijsters, H., 1990. Effects of metals on enzyme activity in plants. Plant Cell Environ. 13, 195 206. Williams, R.J.P., Frausto da Silva, J.J.R., 2002. The involvement of molybdenum in life. Biochem. Biophys. Res. Commun. 292, 293 299.

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C H A P T E R

9 Genetic engineering approaches and applicability for the bioremediation of metalloids Damanjeet Kaur1,2, Ajay Singh3, Abhijit Kumar4 and Saurabh Gupta1 1

Department of Microbiology, Mata Gujri College, Fatehgarh Sahib, India 2Department of Biotechnology, Punjabi University, Patiala, India 3Department of Food Technology, Mata Gujri College, Fatehgarh Sahib, India 4Department of Biotechnology, Chandigarh University, Gharuan, India

9.1 Introduction Global industrialization and geochemical activities lead to the continuous exposure of the environment to various hazardous chemicals. Existence of these unenviable contaminants in the environment beyond the permissible limit adversely affects all living organisms and ecosystems. Among these contaminants, environmental pollution caused by metallic elements is gaining increased attention worldwide. Rapid industrialization and urbanization have increased the contribution of metallic elements in the biosphere. Metals are widespread pollutants of global concern due to their toxicity and persistent nature. These elements constitute a significant proportion of Earth’s crust, and their presence in the mineral pool includes bioavailable metal species with their indispensible role as nutrients for plants and microorganisms. Being important solid components, that is, clays, minerals, oxides of iron, and manganese of soils, these elements play a significant role in the biogeochemical processes of soil (Gadd, 2008). Metals are distinguished from other elements by their significant electrical and thermal conductivity along with malleability, ductility, opacity, and metallic luster (Muller, 2007; Housecroft and Sharpe, 2008). Certain elements have been further categorized into “metalloids” with distinguished physical and

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chemical properties. Elements such as boron, silicon, germanium, arsenic, antimony, and tellurium are referred to as “metalloids or semimetals,” which exhibit properties of both metals and nonmetals. Metalloids have physical properties and appearance like metals but behave chemically like nonmetals (Duffus, 2002). “Heavy metals” is a collective term generally used for both metals and metalloids with high atomic weight and atomic density above 5 g/cm3, almost five times greater than water (Hawkes, 1997), whereas light metals such as sodium, magnesium, and potassium have a density that is lower than these elements. Heavy metals are members of a loosely defined subset of elements in the periodic table including d-block elements, lanthanides, and actinides (Babula et al., 2008). Further, these heavy metals can also be defined by various other criteria, including atomic number, chemical properties, and Lewis acid behavior (Duffus, 2002). Some metals play an integral role in various physiological pathways in living organisms as trace elements, while some induce toxicity at higher concentration. Metals often play a vital role in sustaining life. Depending upon biological functions and toxic effects, metallic elements are classified into three distinct classes (Roane et al., 2014): 1. Essential metals are important for metabolism and growth, for example, aluminum (Al), calcium (Ca), cobalt (Co), copper (Cu), iron (Fe), potassium (K), magnesium (Mg), manganese (Mn), molybdenum (Mo), sodium (Na), nickel (Ni), selenium (Se), vanadium (V), tungsten (W), and zinc (Zn). These metals and metalloids play a major role in normal body functions and pose toxic effects when daily uptake exceeds certain limits, for example, in the case of Cu and Se. 2. Toxic metals and metalloids, for example, silver (Ag), arsenic (As), gold (Au), germanium (Ge), cadmium (Cd), chromium (Cr), mercury (Hg), lead (Pb), antimony (Sb), and tin (Sn), are even lethal at low concentrations. These metals are nonessential elements with no reported biological role so far. 3. Nontoxic nonessential metals, for example, rubidium (Rb), cesium (Cs), strontium (Sr), and titanium (Ti), have no known biological function. Essential metal elements play crucial roles in various life processes of all organisms as these act as catalysts for redox reactions (e.g., iron, copper, and nickel), help to stabilize biomolecules through electrostatic interactions (e.g., magnesium and zinc), act as components of various enzymes (e.g., iron, magnesium, nickel, and cobalt), and regulate osmotic pressure (sodium and potassium) (Nies, 1992; Bruins et al., 2000). However, all the metals, either essential or nonessential, exhibit varied levels of toxic effects and health issues at increased concentrations. Besides their impact on the animal and human body, these toxic metals also play a significant role in physiological activities on soil microbial population. Broadly, three mechanisms have been proposed for the toxic effects of the metals on the biological systems: 1. blocking of the active sites and essential functional groups in enzymes and transport system of an organism; 2. leads to the removal of essential elements from their native binding sites in biomolecules through displacement and/or substitution; and 3. modification of native confirmation state of biological molecules (Connell, 2005).

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9.2 Sources of metals

209

For example, heavy metal ions interact with various physiological ions (Cd21 with Zn21 or Ca21 and Ni21; Co21 with Fe21; Zn21 with Mg21, respectively) inside the cell and inhibit the function of the respective physiological cations. Certain heavy metal cations with high atomic numbers, such as Hg21, Cd21, and Ag21, bind with greater affinity to thiol groups of proteins, thereby inhibiting the activity of enzymes (Nies, 1999). Elevated concentrations of these essential and nonessential metals can (1) damage cell membranes, (2) disrupt the cellular functions, (3) alter enzyme specificity, and (4) damage the DNA structure (Bruins et al., 2000).

9.2 Sources of metals Presence of heavy metals and metalloids in an ecosystem has considerable economic and environmental significance. Metal pollutants are generated through various natural processes and anthropogenic activities and are continuously released into the atmosphere, soil, and water at potentially harmful levels (Avery, 2001). Natural sources, such as volcanic eruptions, geothermal activities, soil erosion, and weathering of metal-enriched rocks, add a significant amount of toxic metals into the environment. Excessive amounts of Al, Zn, Mn, Pb, Ni, Cu, and Hg are emitted by volcanic emissions (Seaward and Richardson, 1990). Apart from natural sources, various anthropogenic activities (Table 9.1), such as TABLE 9.1 Various anthropogenic sources of toxic metals and metalloids in the environment (Dixit et al., 2015; Gautam et al., 2016; Oves et al., 2016). Toxic metals/ metalloids

Sources

Lead

Metalliferous mining and smelting, atmospheric deposition, agriculture, petroleum refining, textile dyeing and printing, pesticides and fertilizer industry, coal burning, sewage sludge, leaded gasoline, and batteries’ waste

Mercury

Electrolysis, petroleum refining, wood preservatives, leather tanning, adhesives and paints, medical waste, mining, smelting and coal combustion, and pesticides

Cadmium

Atmospheric deposition, paint industry, plastics, refined petroleum products, metal smelters, electroplating, leather tanning, industrial waste, pesticides, and fertilizers

Arsenic

Automobile exhaust/industrial dust, wood preservatives, dyes, petroleum refining, agrochemicals, semiconductors, mining, and smelting

Chromium

Petroleum refining, electroplating industry, tanneries, steel industry, fly ash, atmospheric deposition, textile manufacturing, and pulp-processing units

Nickel

Galvanization, automobile batteries, electroplating, paint industry, metal refining, industrial effluent, and chemical and fertilizer industry

Copper

Ore mining and smelting, electroplating industry, plastic industry, pesticide and fertilizer industry, metal refining, and petroleum refining

Zinc

Rubber industries, paint and dyes, leather tanning, wood preservatives, batteries, electroplating industries, fertilizers, and pesticides

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atmospheric deposition, combustion of fossil fuels, electroplating, steel manufacturing, smelting process, mining of metalliferous ores, wastes of municipal areas, leather tanning, chemical processing, aerospace and atomic energy installation, electronic and automobile wastes, and agricultural activities, are also adding vast amounts of toxic metals and metalloids into the various components of the ecosystem (Halim et al., 2003; Wang and Chen, 2006; Ahemad and Malik, 2011). Industrial effluents and drainage water discharged huge amounts of waste containing metallic substances into the environment (Aldoobie and Beltagi, 2013). These indiscriminate human activities lead to an important change in the geochemical cycles along with biochemical imbalance of these metallic elements. Finally, these metallic elements enter the food chain through leaching into the soil and natural water bodies and affect the whole ecosystem (Selvin et al., 2009; Nongbri and Syiem, 2012). Metals have a strong affinity to bind with different biological molecules, which leads to the accumulation of these metals in the various tissues and organs of the humans and animal body. Varied concentrations of toxic metals have been reported in soil, sediments, and aquatic environments worldwide by several researchers due to various anthropogenic processes (Table 9.2). Excessive accumulation of bioavailable forms of toxic metals in the soil and aquatic environment leads to uptake by plants and aquatic organisms, thus adversely affecting the food quality and human health (Giller et al., 1998; Muchuweti et al., 2006).

9.3 Metals: occurrence, speciation, and toxic effects Although certain metals, such as copper (Cu), zinc (Zn), iron (Fe), manganese (Mn), molybdenum (Mo), nickel (Ni), and cobalt (Co), are required by plants and animals and act as essential micronutrients (Reeves and Baker, 2000; Wintz et al., 2002), excessive uptake of these micronutrients by plants leads to toxic effects (Blaylock and Huang, 2000; Monni et al., 2000). All metals, whether of natural or anthropogenic origin, exhibit a wide range of toxicities toward soil microbial populations at higher concentrations, and almost every index of microbial activity is being affected. However, toxicities of these metals depend upon the physicochemical and biotic factors, concentration, bioavailability, and speciation of metal ions (Gadd, 2009). Metals such as lead, cadmium, mercury, arsenic, chromium are of immediate concern due to their toxicity and carcinogenicity. Exposure to these heavy metals even at low concentration induces multiple organ damage (Rehman et al., 2017). Metallic elements exhibit acute and chronic toxicity depending upon type speciation and the concentrations of the metals. Toxicity of these elements occurs by binding to the functional groups present in proteins and nucleic acids. Binding of heavy metals with proteins and nucleic acids induces the generation of reactive oxygen species (ROS) and oxidative stress, which play a key role in the carcinogenicity and toxicity of metal ions (Tchounwou et al., 2012). Upon exposure at elevated levels, toxic metals and metalloids can damage liver, heart, kidney, brain, and lungs and also disrupt processes of immune system, respiratory system, endocrine, gastrointestinal system, and peripheral and central nervous system, thus resulting in various life-threatening diseases and disorders (Jarup, 2003).

Plant Life under Changing Environment

TABLE 9.2 Varied concentrations of metal ions reported in different environmental sources. Location

Metal

Concentration

References

Otago Harbour sediment, New Zealand

Cr

7000 μg/g

Johnson et al. (1981)

Toyohira River, Japan

Cu

22 μg/g

Sakai et al. (1986)

Pb

24 μg/g

Cd

0.20 μg/g

Zn

152 μg/g

Clark Fork River sediment, Montana, United States

As

100 μg/g

Moore et al. (1988)

Godavari River, India

Zn

233.41 μg/L

Sudhakar et al. (1991)

Mn

157.91 μg/L

Cu

879.50 μg/g

Pb

193.5 μg/g

Zn

762.5 μg/g

Cr

155 6 13 mg/kg

Mn

320 6 15 mg/kg

Cr

210 6 15 mg/kg

Mn

500 6 20 mg/kg

Cu

22.2 μg/g

Pb

60.3 μg/g

Cd

9.5 μg/g

Zn

59.2 μg/g

As

4.6 17.8 mg/kg

Cd

0.01 0.12 mg/kg

Cr

6.54 78.4 mg/kg

Cu

0.7 14.9 mg/kg

Hg

0.001 0.049 mg/kg

Ni

2.6 34.9 mg/kg

Pb

10.4 36.7 mg/kg

Zn

6.3 109 mg/kg

Cd

3.90 6 0.25 μg/g

Cr

0.44 6 0.05 μg/g

Ni

0.33 6 0.01 μg/g

Mn

1.1 6 0.11 μg/g

Pb

16.78 6 0.21 mg/L

Cd

5.12 6 0.18 mg/L

Cu

4.90 6 0.25 mg/L

Ni

2.11 6 0.12 mg/L

Quebec, Canada

Buyak Menderes River, Turkey

Gediz River, Turkey

Yamuna River, India

Changhua River, China

Bay of Bengal, India

Nairobi Dam, Kenya

Couillard and Zhu (1992)

Akcay et al. (2003)

Akcay et al. (2003)

Jain (2004)

Hu et al. (2013)

Lakshmanasenthil et al. (2013)

Ndeda and Manohar (2014)

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9.3.1 Lead Lead (Pb) is a natural, bluish-gray metal present in low concentrations in the soil. It is one of the most hazardous and ubiquitously distributed metals present on the Earth. Lead has a bright luster, is highly malleable, ductile, soft, has resistance to corrosion, and is a poor conductor of electricity. In nature, lead exists in four stable isotopes: 204Pb (1.4%), 206 Pb (25.2%), 207Pb (21.7%), and 208Pb (51.7%) (O’Neil, 2003). It is widely used in lead acid batteries, pesticides, ammunitions, metal products, gasoline additives, etc. Human activities, such as mining, smelting, fossil fuel combustion, and sewage sludge, are adding significant amount of lead, which results in the accumulation of the metal into the environment (Huang et al., 2006) from where it enters the food web and poses a threat to living organisms. Due to human intervention, lead is released in the environment in various forms such as elemental lead, lead oxide and hydroxide, and lead metal oxyanion complexes. Naturally, lead exists in both elemental and oxidized states, that is, Pb(0) and Pb(II). Divalent lead is the most stable and reactive form of Pb, which leads to the formation of mononuclear and polynuclear oxides along with hydroxides (Smith et al., 1995). It 22 32 also reacts with both inorganic (Cl2 ; CO22 3 ; SO4 ; PO4 ) and organic ligands (humic and fulvic acids, ethylene diamine tetraacetic acid (EDTA), amino acids) to form low solubility compounds (Bodek et al., 1988). Highly insoluble lead compounds are lead phosphates, lead carbonates (above pH 6), and lead oxides and hydroxides. However, the soluble form of lead is highly hazardous for the environment and ecosystem besides living beings as compared to immobilized lead (Chen et al., 2003). Lead is an extremely toxic metal element with a wide range of biological effects in all organisms, depending upon the concentration of lead and duration of contact with the living being. Uptake of lead in humans and animals occurs mainly through inhalation, ingestion, and absorption via skin (Wuana and Okieimen, 2011). High dose of lead causes severe damage to the central nervous system, liver, kidneys, endocrine system, cardiovascular system, reproductive system, and hematopoietic system (Pirkle et al., 1998; Flora, 2002). Prolonged exposure can result in loss of appetite, headache, hypertension, renal dysfunction, fatigue, sleeplessness, arthritis, hallucinations, intellectual disability, birth defects, psychosis, anemia, autism, allergies, dyslexia, weight loss, hyperactivity, muscular weakness, paralysis, and even death (Papanikolaou et al., 2005). Further lead uptake disturbs the various physiological processes in plants. It significantly affects the photosynthetic process, inhibits enzymes, and induces oxidative stress by increasing the production of ROS, thus suppressing the overall growth of the plants (Stiborova et al., 1987; Reddy et al., 2005).

9.3.2 Mercury Mercury (Hg), also called liquid silver, is a naturally occurring, highly toxic and persistent and bioaccumulative metal present in the environment. Mercury exists in three oxidation states: elemental [Hg(0)], mercurous [Hg(I)], and mercuric [Hg(II)]. It is often used in batteries, thermostats, dentistry, wood processing, nuclear reactors, paper and pulp industry, vaccines, pharmaceutical products, etc. The maximum permissible limit of mercury in drinking water and soil is 2 μg/L and 10 300 μg/kg, respectively (Kumar and Gunasundari, 2018). Mercury exists in three forms: elemental mercury [Hg(0)],

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inorganic salts (mercurous chloride, mercuric chloride, mercuric acetate, and mercuric sulfide), and organic mercury compound (ethylmercury, methylmercury). Each of the individual forms of mercury possesses varied level of toxicities and bioavailability. In its elemental form, mercury exists as a liquid. Elemental mercury is released into the environment in the gaseous state by various natural processes such as volcanic emissions, soil erosion, and geothermal activities (WHO, 2003). Besides natural processes, various human activities also discharge huge amounts of mercury and its compounds into the environment, and these compounds finally enter the food chain through their natural sinks. Among all, coal combustion is the major source of mercury pollution. Inhalation of mercury vapor can cause acute corrosive bronchitis, interstitial pneumonitis, and damage to digestive system, immune system, lungs, kidneys, and central nervous system (Haddad and Stenberg, 1963; Clarkson and Magos, 2006). Mercury compounds are highly lipophilic and can easily cross the blood brain barrier and placenta (Clarkson, 1993). Methylmercury is more toxic than inorganic mercury salts due to its ability in bioaccumulating in tissues of living organisms. Exposure to mercury and its compounds results in numerous disorders such as acrodynia, allergy, gingivitis, congenital malformation, Minamata disease, stomatitis, emotional lability, insomnia, memory loss, and neurological disorders (Clarkson, 1997; Weiss et al., 2002; WHO, 2003; Mohammed et al., 2011). At elevated levels, mercury gets accumulated in aquatic and higher plants, interferes with the photosynthetic process, and induces oxidative stress in plants (Kamal et al., 2004; Israr et al., 2006; Zhou et al., 2007). Besides this, mercury binds specifically with certain functional groups present in proteins along with reactive ions of adenosine diphosphate (ADP) and adenosine triphosphate (ATP) which leads to impairment of several functions associated with these biomolecules (Patra and Sharma, 2000; Patra et al., 2004).

9.3.3 Cadmium Cadmium (Cd) is a soft, lustrous, silver-white, ductile, and malleable metallic element. Cadmium is a transition metal present in the d-block of the periodic table. It is widely distributed in Earth’s crust at an average concentration of about 0.1 0.2 mg/kg. Cadmium is a highly toxic metal even at low concentrations. Weekly intake of 5.8 μg of cadmium/kg of body weight has been reported as harmless by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) (WHO, 2011). Cadmium exists in eight stable isotopes: 106Cd (1.22%), 108Cd (0.88%), 110Cd (12.39%), 111Cd (12.75%), 112Cd (24.07%), 113Cd (12.26%), 114 Cd (28.86%), and 116Cd (7.58%), and the most common are 112Cd and 114Cd (Adriano, 2001a,b). Cadmium exists in the Cd(II) oxidation state and has strong affinity for anionic groups. Cadmium has been widely exploited as alloys, in electroplating industry, in polyvinyl plastics as stabilizers, as pigments, and as the electrode in rechargeable Ni Cd batteries (Wilson, 1988; Adriano, 2001a,b). Volcanic eruption is the major natural source of cadmium release in the environment, although it can also be recovered as a by-product from sulfide ores of lead, zinc, and copper. Cadmium compounds also enter the surroundings through various agricultural activities, industrial discharges, and sewage sludge, which further add to the contamination of soil and water bodies. Primary source of Cd

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exposure in humans is through food and smoking (Singh and McLaughlin, 1999). Cigarette smoking significantly increases the levels of cadmium in the blood, concentrations in smokers being on average found around 4 5 times higher than those in nonsmokers (Jarup et al., 1998). Cd(II) binds with sulfhydryl groups in proteins and other biomolecules. Furthermore, cadmium exposure can result in an increase in the generation of ROS, which in turn induces DNA damage and interferes with the cell-signaling pathway. Cadmium also induces genomic instability and mutations by the inhibition of DNA repair mechanisms (Filipic, 2012). International Agency for Research on Cancer (IARC) also placed cadmium in the category of potential carcinogens (IARC, 1993). Upon exposure, cadmium causes obstructive lung disorders, kidney damage, liver damage, nausea, vomiting, autoimmune diseases, pneumonitis, nervous system failures, abdominal cramps, dyspnea, and muscular weakness (Clarkson et al., 1983; Seidal et al., 1993; Jarup et al., 1998; Satarug and Moore, 2004; Godt et al., 2006). Exposure to elevated levels of cadmium and its compounds also causes itai-itai (ouch-ouch) disease, characterized by osteomalacia, spontaneous fractures, osteoporosis, renal tubular dysfunction, and intense bone-associated pain (Friberg et al., 1971; Chang et al., 1996; Nordberg et al., 2002; Aoshima, 2016).

9.3.4 Arsenic Arsenic (As) is an extremely toxic metalloid that is found abundantly in minerals, rocks, soil, water, air, and in the atmosphere. These are widely dispersed in the Earth’s crust at an average concentration of about 2000 μg/kg. Arsenic has been recognized as a class I carcinogen by the IARC as these exhibit acute and chronic toxicity depending on the type of exposure (Hettick et al., 2015). Arsenic is found in four stable oxidation states: arsenide [As(-III)], elemental [As(0)], arsenite [As(III)], and arsenate [As(V)]. Arsenic is being extracted from processing of ores such as copper, zinc, lead, silver, and gold. Arsenic compounds are widely used as biocontrol agents in agriculture, and also as therapeutic agents, wood preservatives, alloys, pigments, and animal feed additives (Antman, 2001; Cullen, 2008; Saha and Orvig, 2010). Arsenic is introduced into the environment at elevated levels from both natural and anthropogenic activities such as volcanic emissions, mining, smelting of nonferrous metals, coal combustion, and also from arsenic-based pest-/herb-control agents. Arsenic exists in both organic and inorganic forms in the environment. In natural water, mostly the inorganic form is found as oxyanions of trivalent (AsO2 2 ) and pentavalent arsenic (AsO32 4 ) (Smedley and Kinniburgh, 2002; Fekih et al., 2018). Toxicity of arsenic depends upon the oxidation state, chemical form, and solubility. However, the inorganic forms of arsenic are much more hazardous and result in serious health issues such as cancer of skin, lung, liver, kidney, and bladder and also several cardiovascular and neurological diseases (Basu et al., 2014). Long-term exposure of drinking water resources with arsenic poses a significant threat to human health (Mazumder, 2000). Due to health hazards and carcinogenicity-associated arsenic, its permissible limit in public water supplies has been reduced from 0.05 to 0.01 mg/L by the World Health Organization (Masih et al., 2009). Water resources in Argentina, Bangladesh, Canada, China, India, Vietnam,

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Mexico, Laos, United States, and several other countries have been reported with arsenic above threshold limits (Basu et al., 2014). Arsenite (trivalent arsenic) compounds are considered to be more toxic than arsenate (pentavalent arsenic) due to their reactivity with sulfur compounds and generation of ROS (Hughes et al., 2011). Being genotoxic, these metalloids induce deletion mutations, oxidative DNA damage, DNA strand breaks, sister chromatid exchanges, chromosomal aberrations, aneuploidy, and genomic instability (Hei et al., 1998; Basu et al., 2001; Rossman, 2003). Acute exposure with increased concentration of arsenic leads to multiorgan failure, renal failure, respiratory failure, brain damage, anemia, leukopenia, diarrhea, hemolysis, hepatomegaly, melanosis, and damage to the peripheral and central nervous system (WHO, 2001; ATSDR, 2007).

9.3.5 Chromium Chromium is a silvery, lustrous, hard, and brittle metal belonging to the d-block of the periodic table. Chromium plays an integral role in the biological system, but beyond a threshold level, it exhibits toxic, mutagenic, carcinogenic, and teratogenic properties (Asmatullah and Shakoori, 1998; Gili et al., 2002; Codd et al., 2003; Balamurugan et al., 2004). Chromium is a naturally occurring element having different oxidation states from (-II) to (VI) and occurs mostly in Cr(0), Cr(III), and Cr(VI) states. Trivalent chromium compounds are relatively stable and benign, while hexavalent compounds are highly toxic (Adriano, 2001a,b). Cr(III) is relatively immobile in water bodies due to its low solubility. It is an essential micronutrient required for the metabolism of glucose, lipid, and protein at a concentration below 5 ppm but can be toxic and mutagenic at higher concentrations (Bailar, 1997; Shen and Wang, 1993). However, hexavalent chromium is a severe hazard because of its high solubility and strong oxidizing ability (Flora et al., 1990). Chromium is widely exploited in leather tanning, as catalysts in dyeing, pigments, textiles, metal ceramics, as alloys in stainless steel, and as wood preservatives. However, waste discharges from these industries add huge amounts of hexavalent chromium into the soil and aquatic environment and pose a significant threat to aquatic life. Further exposure with chromium compounds occurs through ingestion of food and water and also via inhalation, as increased risk of Cr-induced diseases has also been found in industrial workers, occupationally exposed with chromium (Langard and Vigander, 1983). Widespread incidences of dermatitis were reported among construction workers due to exposure with chromium present in cement (Shelnutt et al., 2007). Extremely high levels of chromium compounds resulted in severe respiratory, gastrointestinal, hematological, cardiovascular, hepatic, renal, and neurological effects (ATSDR, 2012).

9.4 Remediation of toxic metals and metalloids Metal contamination has become a major and widespread problem these days. Discharge of these toxic metal ions into the surroundings without appropriate and effective treatment measures poses a considerable threat to the public health and ecosystem

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due to their recalcitrant and persistent nature. Remediation of metals from contaminated sites is quite challenging as metal elements cannot be degraded by physical, chemical, or biological means to an innocuous by-product. Elimination of toxic metals from the contaminated soil and water is crucial for environmental protection. Reclamation of these polluted sites is one of the major challenges for sustainable development. Various physical, chemical, and biological processes are being used extensively to remove metal pollution from the surroundings. Several microbial or chemical redox processes transform the oxidation state of the metals. Such redox-based remediation processes alter the chemical speciation, solubility, bioavailability, mobility, and toxicity of the metal ions, but the elemental nature of the contaminants remains the same (Borch et al., 2010). To get rid of these toxic contaminants, different physical and chemical techniques, such as precipitation, oxidation reduction, filtration, ion exchange, reverse osmosis, electrochemical treatment, evaporation, and membrane separation, have been widely exploited (Yan and Viraraghavan, 2001). However, these conventional techniques become ineffective and uneconomical for the reduction of metal contaminants present in low concentrations such as below 0.1 g/L (Ahluwalia and Goyal, 2007). Further, these remediation processes also generate a huge amount of toxic chemical sludge and thus can cause disposal problems and also destroy the fertility of soil, adversely affecting its physical structure. Moreover, these technologies are neither cost-effective nor efficient, as these require expensive operational infrastructure and high energy inputs. Due to these drawbacks and limitations associated with physical and chemical remediation practices, biological remediation processes have emerged as effective and inexpensive alternatives for the decontamination of polluted sites.

9.5 Bioremediation The term “bioremediation” is derived from two words: “bio” means living organisms and “remediate” refers to remedy. Bioremediation refers to the decontamination of the contaminated environment by using living organisms. Bioremediation can be defined as a process in which hazardous wastes are degraded biologically to a less toxic form under controlled conditions. Bioremediation is gaining increased importance as an alternate technology for the effective cleanup of polluted sites. Bioremediation is a multidisciplinary approach, which utilizes the intrinsic metabolic capability of biological entities for the degradation or transformation of pollutants from the contaminated sites. The biological entities could be indigenous flora in the contaminated site or could be added to it from elsewhere (Vidali, 2001). Use of microbes provides a safe and economic alternative to physiochemical technologies. Slow degradation and transformation of toxic contaminants lead to their accumulation in the environment, hence posing severe hazard to both biotic and abiotic environments. Thus biological remediation has emerged as the most advantageous technique for the treatment of metal- and organic pollutant contaminated soil and groundwater. Bioremediation is operated both in situ and ex situ, depending on the nature of contaminants and site conditions (Alvarez and Illman, 2006; Sardrood et al., 2013).

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9.5.1 Ex situ bioremediation It involves the physical excavation of contaminants from their site of origin and subsequent transport to another site for treatment. Ex situ bioremediation is quite fast and is used extensively for the treatment of a wide array of contaminants. Efficacy of ex situ bioremediation depends upon various factors such as type of pollutants, geographical location, and degree of pollution. Depending upon the state of contaminant, ex situ bioremediation can be classified as follows: 9.5.1.1 Slurry-phase bioremediation It is a controlled treatment system in which aqueous suspension of contaminants is remediated in a bioreactor under optimum environmental conditions. Slurry-phase bioremediation is a relatively fast process. 9.5.1.2 Solid-phase bioremediation This system is used for the remediation of solid contaminants, including organic waste, domestic, agricultural, and industrial waste, animal dung, sewage sludge, and municipal solid waste.

9.5.2 In situ bioremediation In situ remediation is the treatment of pollutants at the site of their origin, thus resulting in minimal disturbance and disruption. These techniques are cheaper as compared with other bioremediation technologies, as no additional cost is required for the excavation and transport of contaminants. In situ bioremediation is distinguished into two types: 9.5.2.1 Intrinsic in situ bioremediation Degradation of contaminants with the intrinsic capability of indigenous microbes without any stimulation or treatment is called intrinsic in situ bioremediation. This remediation technique is also known as natural attenuation. 9.5.2.2 Engineered in situ bioremediation It involves the manipulation of physiochemical conditions for accelerating the growth and activities of microorganisms, thus stimulating the degradation process.

9.5.3 Bioremediation technologies The bioremediation process can be facilitated by various techniques such as bioventing, biosparging, bioaugmentation, bioslurping, biofilters, biostimulation, land farming, and composting (Vidali, 2001; Mudhoo and Mohee, 2012; Sardrood et al., 2013; Azubuike et al., 2016; Choudhary et al., 2017). 9.5.3.1 Bioventing Bioventing is a type of in situ bioremediation technique that stimulates the aerobic degradation process. It enhances the intrinsic capability of indigenous microflora to degrade

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the organic contaminants adsorbed to soil by introducing oxygen into an unsaturated zone. Air is circulated by direct air injection into the contaminated zone through vertical and horizontal wells. This technique utilizes only the required amount of air that is necessary for degradation. It also minimizes the volatilization and discharge of contaminants into the environment. 9.5.3.2 Biosparging Biosparging is also an in situ bioremediation method in which aeration under pressure is done beneath the water table for increasing groundwater oxygen concentrations, thus boosting up the degradation of pollutants by indigenous microbes. This technique is quite similar to air sparging in the separation of volatile compounds via desorption and volatilization from the saturated zone. Pressurized air causes volatile compounds to move upward toward unsaturated zone, thus enhancing the degradation process. 9.5.3.3 Bioaugmentation Bioaugmentation is the process of introduction of a specific combination of naturally occurring or genetically engineered microbial strains having enhanced capabilities in contaminated sites for augmenting the natural degradation process (Andreolli et al., 2015). Bioaugmentation is employed for remediating soil and groundwater contaminated with chlorinated ethene such as tetrachloroethylene and trichloroethylene. 9.5.3.4 Bioslurping Bioslurping is an in situ bioremediation process, which combines the efficiency of vacuum-enhanced pumping, soil vapor extraction together with bioventing for the treatment of soil, and groundwater contaminated with volatile and semivolatile organic compounds. 9.5.3.5 Biofilters Biofilters are used to degrade contaminants present in air emissions by immobilizing microorganisms on a solid support. When air pollutants are passed through biofilters, these get adsorbed onto microbial biofilms and are thus degraded sequentially. Biofilters are used for removing sulfur gases, hydrogen sulfide, ethyl benzene, dimethyl sulfides, nitrous oxide, etc. from the air. 9.5.3.6 Biostimulation Biodegradation abilities and the growth of indigenous microbial populations are stimulated by the addition of various aqueous solutions, having nutrients or other amendments, to the contaminated site. This technique has been designed for the bioremediation of soil and groundwater, containing hydrocarbons, volatile organic compounds, pesticides, herbicides, etc. 9.5.3.7 Land farming This technique involves the bioremediation of the polluted soil above ground. For this, the contaminated soil is excavated and mixed with microbes, nutrients, and other amendments, followed by spreading over a prepared bed to facilitate aerobic degradation of

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contaminants. Soil is periodically tilled until remediated completely. It is a simple bioremediation technique, which can be operated both as in situ and ex situ. 9.5.3.8 Composting Composting is a degradation technique in which organic contaminants are converted to a humus-like substance by microbial species at elevated temperature under both aerobic and anaerobic conditions. Contaminated soil is added with nonhazardous organic waste, such as animal waste, agricultural waste, or manure, for the growth of microbial-rich population. Composting can be carried out by using aerated piles, static piles, or continuousfed reactor. Despite toxic stress, microbes play an important role in the global cycling of these toxic metal elements present in nature. Numerous microbial strains have also evolved certain chromosomally or extrachromosomally (plasmid) controlled metal-detoxification mechanisms for neutralizing the deleterious effects of toxic metallic compounds (Silver and Phung, 1996). These mechanisms either prevent the entry of metal ions into the cell or actively efflux these by highly specified systems encoded by different resistance genes. The detoxification of metals can be attributed by different pathways such as biosorption, intracellular assimilation, immobilization, extracellular precipitation, intracellular/extracellular sequestration, efflux, oxidation/reduction reactions, methylation/demethylation, extracellular detoxification, and volatilization (Giller et al., 1998; Lloyd, 2002; Gadd, 2010). Highly resistant bacterial strains have been isolated and characterized from contaminated sites and explored for their ability to detoxify toxic metal ions. Numerous microbial strains, such as Pseudomonas, Alcaligenes, Bacillus, Lysinibacillus, Enterobacter, Penicillium, and Aspergillus, have been reported for the efficient transformation of toxic metals into less toxic forms by several researchers enlisted in Table 9.3. However, the detoxification mechanisms vary with strain and speciation of the metal. Bioremediation is quite simple, inexpensive, and an eco-friendly technique for restoring contaminated sites. Bioremediation offers an attractive, sustainable, and novel technology that is much more efficient in eliminating hazardous contaminants from the environment than the conventional practices. Compared with physical and chemical remediation processes, bioremediation techniques are more acceptable in achieving high efficiency of detoxification along with low cost and minimum disposable sludge volume. Further, these biomass-based remediation processes also offer the development of a nondestructive desorption technique for biomass restoration and quantitative metal recovery (Eapen and D’Souza, 2005).

9.6 Phytoremediation Phytoremediation is a plant-based remediation process, which explores the remarkable capacity of plants in concentrating elements and compounds from the environment and metabolizing these into their tissues (Salt et al., 1998). It is the use of plants to extract, sequester, and detoxify contaminants from the environment. Phytoremediation is an emerging, highly effective, inexpensive, nonintrusive, and eco-friendly approach for the

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TABLE 9.3 Detoxification of toxic metals (lead, arsenic, cadmium, chromium, and mercury) by different microbial species. Metal Microbial species Pb

As

Cd

Cr

Detoxification mechanism

References

Pseudomonas, Alcaligenes, Acinetobacter, Flavobacterium, Aeromonas

Biomethylation

Wong et al. (1975)

Penicillium chrysogenum

Biosorption

Niu et al. (1993)

Citrobacter freundii, Staphylococcus aureus

Intracellular precipitation

Levinson and Mahler (1998)

Enterobacter sp. J1

Biosorption

Lu et al. (2006)

Pseudomonas aeruginosa BS-2

Biosurfactant production

Juwarkar et al. (2007)

Bacillus sp. RS-1, RS-2, and RS-3

Intracellular sequestration

Gupta et al. (2014)

Microbacterium lacticum

Oxidation

Mokashi and Paknikar (2002)

Exiguobacterium sp. WK6 Aeromonas sp. CA1

Reduction

Anderson and Cook (2004)

Pseudomonas sp. As-1

Reduction and efflux

Patel et al. (2007)

Brevibacillus brevis

Oxidation

Banerjee et al. (2013)

Bacillus cereus

Biosorption

Giri et al. (2013)

Pseudomonas stutzeri

Oxidation and reduction

Zhang et al. (2016)

P. aeruginosa

Extracellular precipitation, sulfide production

Wang et al. (1997)

Bacillus thuringiensis DM55

Biosorption

El-Helow et al. (2000)

Pseudomonas sp. H1, Bacillus sp. H9

Reduction

Roane et al. (2001)

Arthrobacter D9, Pseudomonas sp. I1a

Extracellular sequestration

Enterobacter sp. J1

Biosorption

Lu et al. (2006)

P. aeruginosa BS-2

Biosurfactant production

Juwarkar et al. (2007)

Alcaligenes sp.

Biosorption and intracellular sequestration

Kumar et al. (2012)

Streptomyces sp. R22 and R25

Reduction

Amoroso et al. (2001)

Aspergillus niger

Reduction

Park et al. (2005)

Cyberlindnera fabianii, Wickerhamomyces anomalus, Candida tropicalis

Biosorption

Bahafid et al. (2013)

Pseudochrobactrum saccharolyticum LY10

Reduction

Long et al. (2013)

Cellulosimicrobium sp.

Reduction

Bharagava and Mishra (2018) (Continued)

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TABLE 9.3 (Continued) Metal Microbial species Hg

Detoxification mechanism

References

Klebsiella pneumoniae

Reduction and volatilization

Zeroual et al. (2001)

P. aeruginosa, K. pneumoniae

Volatilization

Dzairi et al. (2004)

B. cereus MM08, Lysinibacillus sp. HG17, Bacillus sp. CM111, Kocuria rosea EP1, Microbacterium oxydans HG3, Serratia marcescens HG19, Ochrobactrum sp. HG16

Biosorption and extracellular sequestration

Francois et al. (2012)

Lysinibacillus fusiformis

Sequestration and volatilization

Gupta et al. (2012)

Alcaligenes faecalis

Sequestration, reduction, and volatilization

Gupta and Nirwan (2015)

Yarrowia spp. Idd1 and Idd2

Bioaccumulation, extracellular microprecipitation, and volatilization

Oyetibo et al. (2016)

remediation of polluted soils (Garbisu et al., 2002; Alkorta et al., 2004). It can be operated in situ, thus reducing the soil disturbance and spread of pollutants. Various compounds, including both organic and inorganic pollutants, such as xenobiotics, pesticides, heavy metals, and hydrocarbons, can be effectively remediated by plants. Moreover, remediation of contaminated environments can be carried out by both naturally occurring and genetically engineered plants (Flathman and Lanza, 1998). Phytoremediation is regarded as a safe, economical, and long-term strategy for the remediation of toxic metal contaminated soil. Phytoremediation involves several mechanisms, such as phytodegradation, phytostimulation, phytostabilization, phytovolatilization, phytoextraction, and rhizofiltration, depending upon the nature and type of the pollutant (Salt et al., 1995, 1998; Abou-Shanab, 2011):

9.6.1 Phytodegradation Phytodegradation is the breakdown or degradation of organic contaminants by enzymes produced by the plants.

9.6.2 Phytostimulation Phytostimulation is also called rhizodegradation or plant-assisted bioremediation. It is the degradation of organic contaminants by soil-dwelling microbes. Plants liberate certain microbial growth promoting substances in the soil, which results in enhanced microbial activity along with significant degradation of contaminants.

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9.6.3 Phytostabilization Phytostabilization reduces the bioavailability and mobility of pollutants in the environment through immobilization of contaminants from soil and water systems by plant roots, hence restricting their entry in the biological system and food chain.

9.6.4 Phytovolatilization Phytovolatilization is a process in which plants uptake contaminants from the soil or water, and volatilize these and release less toxic forms in the atmosphere through transpiration.

9.6.5 Phytoextraction Phytoextraction, also known as phytoaccumulation, involves the use of hyperaccumulating plants for the extraction and translocation of heavy metals from the contaminated soil to harvestable plant parts (leaves, shoots, etc.). Harvested plant parts can be ashed or utilized for metal recovery, followed by the disposal of ashes in the landfills.

9.6.6 Rhizofiltration Rhizofiltration is similar to phytoextraction but is mainly concerned with the remediation of polluted groundwater rather than the soil. It involves the use of plant roots to absorb, concentrate, and precipitate contaminants from water and aqueous waste streams. Plant roots act as a filter for the adsorption of contaminants. Hyperaccumulators are defined as the species capable of accumulating metals at a level 100-fold greater than nonaccumulator species. Numerous plant species belonging to families, such as Asteraceae, Brassicaceae, Caryophyllaceae, Cyperaceae, Cunoniaceae, Fabaceae, Flacourtiaceae, Lamiaceae, Poaceae, Violaceae, and Euphorbiaceae, have been identified as natural metal hyperaccumulators with significant metal-accumulating ability (McGrath and Zhao, 2003). Plants, such as Alyssum species, Thlaspi species, Brassica juncea, Viola calaminaria, Astragalus racemosus, are known to accumulate elevated concentrations of heavy metals and radionuclides (Negri and Hinchman, 2000; Reeves and Baker, 2000). Zn and Ni hyperaccumulation was first observed in Thlaspi caerulescens and Alyssum bertolonii (Brassicaceae), respectively (Reeves and Baker, 2000; Kramer, 2010). However, Ni hyperaccumulation has been also reported in Berkheya coddii (Long et al., 2002). A member of Crassulaceae Sedum alfredii has been reported as a Cd and Zn hyperaccumulator plant (Deng et al., 2007). A wild metal accumulator, B. juncea (Indian mustard), has been reported to accumulate and concentrate lead, cadmium, nickel, zinc, copper, and hexavalent chromium in roots and shoots (Kumar et al., 1995). Recently, a fern, Pteris vittata, has been reported as the first arsenic hyperaccumulator by Ma et al. (2001). It has accumulated around 27,000 mg As/kg in the frond dry weight (Wang et al., 2002). Several other fern species, such as Pityrogramma calomelanos, Pteris cretica, Pteris longifolia, and Pteris umbrosa, have been also identified as potential arsenic hyperaccumulators (Francesconi et al., 2002; Zhao et al., 2002).

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9.7 Genetic engineering and its application in the bioremediation of toxic metals Although numerous microbial species exist in the environment for the degradation of toxic contaminants, a majority of these microbes exhibit slow degradation. Presence of various chemical elements in most of the contaminants makes these resistant to biodegradation by microbes. Due to a lack of catabolic pathways required for the degradation of toxic contaminants, it is necessary to enhance the capability of microbial species for detoxifying or degrading the specific contaminant. This can be done by genetic engineering approaches to construct the novel microbial strains, having unique characteristics with broad-spectrum bioremediation potential as compared with indigenous microbes (Kumar et al., 2018). Genetic engineering is the alteration of the characteristics of an organism by manipulating its genetic material using biotechnological tools. Genetic engineering is the process of transfer of gene of interest from one organism to another for obtaining the desired product. Any biological organism whose genetic material has been altered by genetic engineering techniques is termed as a recombinant organism or genetically modified organism. Recombinant bacteria can also be obtained by natural genetic exchange between bacteria. Recent developments in genetic engineering and recombinant DNA technology have enabled the production of novel strains with desirable transformation efficiencies. Genetic engineering is the one of the most important techniques, which can be employed to improve the bioremediation and phytoremediation potential microbes and plants to a great extent. Genetic engineering of the microbes involved in bioremediation practices could improve the process by the introduction of genes responsible for transformation of recalcitrant compounds, or genes specific for degradation pathways. Use of genetically engineered microbes in the bioremediation of toxic compounds has received a great deal of attention as these microbes have higher degradative capacity. The development of genetically engineered microorganisms having bioremediation potential depends upon four principal approaches (Menn et al., 2000): 1. 2. 3. 4.

alteration of enzyme specificity and affinity; construction of specific pathways and their regulation; bioprocess development and its monitoring and control; and application of affinity-based biosensors for chemical sensing, toxicity reduction, and end point analysis.

Recombinant microbes and plants are being receiving enormous attention for the bioremediation of toxic metals. A wide array of genetic determinants associated with metal resistance and detoxification mechanisms has been widely studied among several microorganisms. Some of these resistance systems involve metal-binding proteins or enzymatic transformations, such as oxidation, reduction, methylation, and demethylation, while other systems function by energy-dependent efflux of metal ions. Bacterial plasmids encode for several genes for resistances to many toxic heavy metal ions such as Ag1, Cd21, Co21, 31 1 32 21 22 21 21 21 AsO2 2 ; AsO4 ; Hg ; Cu ; Ni ; Zn ; Sb ; Tl ; TeO3 (Silver and Phung, 2005). By using

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tools and techniques of recombinant DNA technology, genes involved in metal uptake, sequestration, and detoxification strategies can be transferred to a model plant for improved metal-accumulating ability and phytoremediation traits. Overexpression of the desired gene results in increased metal uptake, translocation, and intracellular targeting (Eapen and D’Souza, 2005). Thus genetic engineering of plants and microbes has open up new avenues with enhanced detoxification capabilities.

9.7.1 Mercury Mercury is the extremely toxic and naturally occurring heavy metal present in the environment. Mercury resistance has been widely studied in bacteria. To overcome the toxic effects of mercury, microbes have developed a wide array of resistance or detoxification mechanisms (Osborn et al., 1997): 1. 2. 3. 4. 5.

reduced uptake of mercuric ions; demethylation of methylmercury, followed by conversion to mercuric sulfide; sequestration of methylmercury; methylation of mercury; and enzymatic reduction of Hg(II) to a less toxic form of Hg(0).

Detoxification of mercury is based on the expression of clustered gene of mer operon, can be located on plasmids, transposons (Tn501, Tn21), and bacterial chromosome (Summers, 1986; Osborn et al., 1997; Barkay et al., 2003). Mercury-resistance determinants have been found among both Gram-positive and Gram-negative bacteria. The mer operon contains certain functional genes, promoters, operators, and regulators, and is a positively inducible operon under the control of product of merR gene. The most common functional genes in the mer operon are merA and merB, which encode for mercuric reductase and organomercurial lyase, respectively. Mercuric reductase is a cytosolic flavin disulfide oxidoreductase, which uses NAD(P)H as an electron donor. Detoxification of mercury is mediated by organomercurial lyase, which converts the organomercurial compounds, such as methylmercury and phenylmercuric acetate, into the inorganic form (Hg[II]). Further, mercuric reductase results in the conversion of inorganic mercury into nonbioavailable volatile elemental mercury (Hg[0]), and elemental mercury is then volatilized from the cell. A transconjugant strain Cupriavidus metallidurans MSR33 was engineered by expressing IncP-1b plasmid pTP6, containing novel merB, merG, and other mer genes from heavy metal resistant strain C. metallidurans CH34. The engineered strain exhibited broad-spectrum mercury resistance and detoxified mercury from polluted water (Rojas et al., 2011). Similarly, cloning and expression of mercuric reductase (merA) gene from Hgresistant Escherichia coli into Hg-sensitive E. coli resulted in an elevated mercuric ion reductase activity in host (Zeyaullah et al., 2010). Nicotiana tabacum and Arabidopsis thaliana are the examples of transgenic plants expressing bacterial merA and merB genes with the potential to eliminate mercury from the soil. merA and merB genes have been successfully expressed in A. thaliana. Bizily et al in 2000 reported a significant increase towards

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tolerance of methylmercury along with its biotransformation in less toxic and volatile mercury in genetically modified A. thaliana as compared to wild type. Similarly, mercuric ion reduction and resistance in genetically modified N. tabacum and A. thaliana (Heaton et al., 1998) and Liriodendron tulipifera (Rugh et al., 1998) have been reported.

9.7.2 Arsenic Arsenic is extremely toxic when present in oxidized forms. Microbes have evolved several different cellular mechanisms, such as reduction, active extrusion, extracellular precipitation, or chelation, to cope with arsenic toxicity. Arsenic resistance and detoxification has been documented in several bacteria, including both Gram-positive and Gram-negative bacteria, and are under the control of the ars operon (Cervantes et al., 1994). The ars operon contained three genes: arsR, which encodes for regulatory repressor involved in transcriptional regulation, arsB, which encodes for membrane-bound arsenite permease pump, and arsC, which encodes for intracellular arsenate reductase. The repressor senses the presence of arsenite and controls the expression of ArsB and ArsC proteins. Gene arsC catalyzes glutathione (GSH)-coupled reduction of arsenate (As[V]) to arsenite (As[III]), and ArsB outflows arsenite from cells by functioning as an As(OH)32H1 antiporter (Tripathi et al., 2007). In some Gram-negative bacteria the ars operon contains two additional genes (arsRDABC), that is, arsA, which is an intracellular ATPase, binding to ArsB and converting the As(III) carrier protein into a primary ATP-driven As(III) efflux pump, and arsD has weak As(III)-sensitive transcriptional repressor activity (Rosen, 2002). Bioremediation of arsenic further proceeds through the conversion of these bioavailable forms into volatile arsenic compounds, as arsenite is more toxic than arsenate. Major volatile arsenic compounds formed by the volatilization and biomethylation of arsenic are arsines, mono-, di-, and trimethylarsine. Arsenic volatilization proceeds through the reduction of arsenate to arsenite, followed by its methylation to trimethylarsine as the final product (Bentley and Chasteen, 2002; Turpeinen et al., 2002). Gene arsM located on arsRM operon is regulated by the ArsR-type repressor, which encodes for enzyme arsenite S-adenosylmethionine methyltransferase that mediates methylation of arsenite to volatlite trimethylarsine through intermediate dimethylarsinic acid, monomethylarsonic acid, and trimethylarsine oxide (Qin et al., 2006). Gene arsM (arsenite S-adenosylmethionine methyltransferase) from Rhodopseudomonas palustris was successfully cloned and expressed in E. coli by several researchers. The engineered strain resulted in the methylation of inorganic arsenic to volatile trimethylarsine (Qin et al., 2006; Yuan et al., 2008). Transformation of A. thaliana with genes encoding for arsenic reductase (ArsC) and γ-glutamylcysteine synthetase (γ-ECS) from E. coli resulted in increased tolerance in engineered plants toward arsenic. Further, these engineered plants also show significant increase in arsenic accumulation than wild-type plants and plants with ArsC or γ-ECS alone (Dhankher et al., 2002). Overexpression of arsM gene in Sphingomonas desiccabilis and Bacillus idriensis from R. palustris resulted in 10-fold As volatilization (Liu et al., 2011). Similarly, expression of [As(III)] S-adenosylmethionine methyltransferase

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(arsM) gene in Pseudomonas putida KT2440 was successfully carried out. The resultant transformed strain exhibited volatilization of arsenic into a less toxic form (Chen et al., 2013). Genetically engineered Bacillus subtilis expressing arsenite S-adenosylmethionine methyltransferase gene from thermophilic alga Cyanidioschyzon merolae converted inorganic As into volatile dimethylarsenate and trimethylarsine oxide (Huang et al., 2015).

9.7.3 Cadmium Plants detoxify heavy metals by sequestering through metal-binding peptides called phytochelatin (PC) or their GSH precursor. PCs are naturally occurring cysteine-rich peptides, which have high binding affinity for toxic metals. GSH-dependent PC synthesis is one of the most important mechanisms conferring to Cd accumulation and tolerance. GSH is synthesized from its constituent amino acids in two ATP-dependent enzymatic reactions, catalyzed by γ-ECS and GSH synthetase (GS), respectively. B. juncea (Indian mustard) was genetically engineered to overexpress gshII gene encoding GS (Zhu et al., 1999a), and gshI gene encoding γ-ECS (Zhu et al., 1999b) from E. coli. The transgenic plants showed increased tolerance and accumulation of cadmium as compared to the wild type. Overexpression of γ-ECS and GS increase the biosynthesis of GSH and PCs, which in turn increase the Cd tolerance and accumulation ability of transgenic plants (Zhu et al., 1999a,b). Cloning and expression of manganese transport gene (mntA) and a metalsequestering protein (metallothionein) in E. coli resulted in the rapid accumulation of Cd in an aqueous phase (Kim et al., 2005). Genetic engineering of Acidiphilium multivorum and E. coli with plasmid from Acidocella GS19h strain harbored resistance against zinc and cadmium (Ghosh et al., 1997). Saccharomyces cerevisiae protein YCF1 is a member of the ATPbinding cassette (ABC) transporter, which detoxifies cadmium by transporting it in vacuoles. Overexpression of YCF1 in YCF1 deletion mutant DTY167 and A. thaliana resulted in increased resistance and accumulation of lead and cadmium than wild type (Song et al., 2003). PC synthase (PCS, also known as GSH γ-glutamylcysteinyltransferase, EC2.3.2.15) is an enzyme involved in the synthesis of PCs. Overexpression of PCs from garlic and GSH from baker’s yeast in A. thaliana resulted in increased tolerance and accumulation of Cd and As in transformed plants (Guo et al., 2008). Introduction of PCS gene from Schizosaccharomyces pombe into P. putida KT2440 resulted in recombinant strain KT2440spPCS with increased resistance to cadmium, mercury, and silver. Further, the recombinant strain also displayed three- to fivefold increase in cadmium accumulation over wild type (Yong et al., 2014). Similarly, enhanced tolerance toward cadmium, copper, sodium, and mercury has been observed in transformed E. coli strain overexpressed with PcPCS1 gene from Pyrus calleryana (Li et al., 2015). Cloning of pGIAK1 cad operon and pGIAK1 ars operon from Bacillaceae strain JMAK1 in Bacillus cereus H3081.97 and B. subtilis 1A280 conferred cadmium and arsenic resistances to host strains, respectively (Guo and Mahillon, 2013).

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9.7.4 Lead Lead resistance has been widely reported in both Gram-positive and Gram-negative bacteria. Resistance is conferred by a lead resistance determinant pbr, located on pMOL30 plasmid in Ralstonia metallidurans strain CH34, which is involved in uptake, efflux, and accumulation of lead. The operon contains several structural genes such as pbrT, pbrA, pbrB, and pbrD. pbrT encodes for the protein required for Pb(II) uptake, pbrA encodes for P-type Pb(II) efflux ATPase, pbrB encodes for predicted integral membrane protein, pbrC encodes a predicted prolipoprotein signal peptidase, pbrD encodes for Pb(II) binding protein. A merR-like regulator, pbrR, controls the transcription of pbr structural genes (Borremans et al., 2001). Besides this, CadA ATPase of Staphylococcus aureus and ZntA ATPase of E. coli have also been reported for efflux of Pb (II). CadA is a P-type ATP-coupled Cd(II) pump and ZntA is a Zn(II)/Cd(II) pump (Rensing et al., 1998).

9.8 Conclusion Metal contamination is a major global problem. Both natural and anthropogenic sources have led to the increased mobilization of toxic metals into the biosphere. Bioremediation provides an innovative and effective method for the remediation of metal-contaminated sites. Bioremediation is a widely adopted process, which utilizes the natural ability of microflora. Different conventional and biological remediation technologies have been widely adopted for the treatment, but several drawbacks have further restricted their use. To overcome the limitations associated with these remediation technologies, genetically engineered microbes have been used extensively for the removal of contaminants. Genetic engineering has enabled the modification of microbes and plants with enhanced remediation potential. Exploration of the molecular and genetic basis of toxic metals’ metabolism in microbes has provided an extensive knowledge base for developing proficient and selective bioremediation tools.

References Abou-Shanab, R.A.E.I., 2011. Bioremediation: new approaches and trends. In: Khan, M., Zaidi, A., Goel, R., Musarrat, J. (Eds.), Biomanagement of Metal-Contaminated Soils. Environmental Pollution, vol. 20. Springer, Dordrecht. Adriano, D.C., 2001a. Cadmium. Trace Elements in Terrestrial Environments. Springer, New York. Adriano, D.C., 2001b. Trace Elements in Terrestrial Environments Biogeochemistry, Bioavailability and Risks of Metals, second ed Springer-Verlag. Ahemad, M., Malik, A., 2011. Bioaccumulation of heavy metals by zinc resistant bacteria isolated from agricultural soils irrigated with wastewater. Bacteriol. J. 2, 12 21. Ahluwalia, S.S., Goyal, D., 2007. Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour. Technol. 98, 2243 2257. Akcay, H., Oguz, A., Karapire, C., 2003. Study of heavy metal pollution and speciation in Buyak Menderes and Gediz river sediments. Water Res. 37, 813 822.

Plant Life under Changing Environment

228

9. Genetic engineering approaches and applicability for the bioremediation of metalloids

Aldoobie, N.F., Beltagi, M.S., 2013. Physiological, biochemical and molecular responses of common bean (Phaseolus vulgaris L.) plants to heavy metals stress. Afr. J. Biotechnol. 12, 4614 4622. Alkorta, I., Hernandez-Allica, J., Becerril, J.M., Amezaga, I., Albizu, I., Garbisu, C., 2004. Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev. Environ. Sci. Biotechnol. 3, 71 90. Alvarez, P.J.J., Illman, W.A., 2006. Bioremediation and Natural Attenuation: Process Fundamentals and Mathematical Models. Wiley. Amoroso, M.J., Castro, G.R., Duran, A., Peraud, O., Oliver, G., Hill, R.T., 2001. Chromium accumulation by two Streptomyces spp. Isolated from riverine sediments. J. Ind. Microbiol. Biotechnol. 26, 210 215. Anderson, C., Cook, G., 2004. Isolation and characterization of arsenate-reducing bacteria from arsenic-contaminated sites in New Zealand. Curr. Microbiol. 48, 341 347. Andreolli, M., Lampis, S., Brignoli, P., Vallini, G., 2015. Bioaugmentation and biostimulation as strategies for the bioremediation of a burned woodland soil contaminated by toxic hydrocarbons: a comparative study. J. Environ. Manage. 153, 121 131. Antman, K.H., 2001. Introduction: the history of arsenic trioxide in cancer therapy. Oncologist 6, 1 2. Aoshima, K., 2016. Itai-itai disease: renal tubular osteomalacia induced by environmental exposure to cadmiumhistorical review and perspectives. J. Soil Sci. Plant Nutr. 62, 319 326. Asmatullah, Q.N.N., Shakoori, A.R., 1998. Hexavalent chromium reduction induced congenital abnormalities in chick embryo. J. Appl. Toxicol. 18, 167 171. ATSDR, 2007. Toxicological Profile for Arsenic. U.S. Department of Health & Human Services. Agency for Toxic Substances and Disease Registry, Atlanta, GA. ATSDR, 2012. Toxicological Profile for Chromium. U.S. Department of Health and Human Services. Agency for Toxic Substances and Disease Registry, Atlanta, GA. Avery, S.V., 2001. Metal toxicity in yeasts and the role of oxidative stress. Adv. Appl. Microbiol. 49, 111 142. Azubuike, C.C., Chikere, C.B., Okpokwasili, G.C., 2016. Bioremediation techniques classification based on site of application: principles, advantages, limitations and prospects. World J. Microbiol. Biotechnol. 32, 1 18. Babula, P., Adam, V., Opatrilova, R., Zehnalek, J., Havel, L., Kizek, R., 2008. Uncommon heavy metals, metalloids and their plant toxicity: a review. Environ. Chem. Lett. 6, 189 213. Bahafid, W., Joutey, N.T., Sayel, H., Houssaini, M.I., Ghachtouli, N.E., 2013. Chromium adsorption by three yeast strains isolated from sediments in Morocco. Geomicrobiol. J. 30, 422 429. Bailar, J.C., 1997. Chromium. In: Parker, S.P. (Ed.), McGraw-Hill Encyclopedia of Science and Technology. McGraw-Hill, New York. Balamurugan, K., Rajaram, R., Ramasami, T., 2004. Caspase-3: its potential involvement in Cr(III) induced apoptosis of lymphocytes. Mol. Cell Biochem. 259, 43 51. Banerjee, S., Majumdar, J., Samal, A.C., Bhattachariya, P., Santra, S.C., 2013. Biotransformation and bioaccumulation of arsenic by Brevibacillus brevis isolated from arsenic contaminated region of West Bengal. IOSR J. Environ. Sci. Toxicol. Food Technol. 3, 1 10. Barkay, T., Miller, S.M., Summers, A.O., 2003. Bacterial mercury resistance from atoms to ecosystem. FEMS Microbiol. Rev. 27, 355 384. Basu, A., Mahata, J., Gupta, S., Giri, A.K., 2001. Genetic toxicology of a paradoxical human carcinogen, arsenic: a review. Mutat. Res. 488, 171 194. Basu, A., Saha, D., Saha, R., Ghosh, T., Saha, B., 2014. A review on sources, toxicity and remediation technologies for removing arsenic from drinking water. Res. Chem. Intermed. 40, 447 485. Bentley, R., Chasteen, T.G., 2002. Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol. Mol. Biol. Rev. 66, 250 271. Bharagava, R.N., Mishra, S., 2018. Hexavalent chromium reduction potential of Cellulosimicrobium sp. isolated from common effluent treatment plant of tannery industries. Ecotoxicol. Environ. Saf. 147, 102 109. Bizily, S.P., Rugh, C.L., Meagher, R.B., 2000. Phytodetoxification of hazardous organomercurials by genetically engineered plants. Nat. Biotechnol. 18, 213 217. Blaylock, M.J., Huang, J.W., 2000. Phytoextraction of metals. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals-Using Plants to Clean up the Environment. Wiley, New York.

Plant Life under Changing Environment

References

229

Bodek, I., Lyman, W.J., Reehl, W.F., Rosenblatt, D.H., 1988. Environmental Inorganic Chemistry: Properties, Processes and Estimation Methods. Pergamon Press, Elmsford, NY. Borch, T., Kretzschmar, R., Kappler, A., Van Cappellen, P., Ginder-Vogel, M., Voegelin, A., et al., 2010. Biogeochemical redox processes and their impact on contaminant dynamics. Environ. Sci. Technol. 44, 15 23. Borremans, B., Hobman, J.L., Provoost, A., Brown, N.L., Lelie, D., 2001. Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. J. Bacteriol. 183, 5651 5658. Bruins, M.R., Kapil, S., Oehme, F.W., 2000. Microbial resistance to metals in the environment. Ecotoxicol. Environ. Saf. 45, 198 207. Cervantes, C., Ji, G., Ramirez, J.L., Silver, S., 1994. Resistance to arsenic compounds in microorganisms. FEMS Microbiol. Rev. 15, 355 367. Chang, L.W., Nogawa, K., Kido, T., 1996. Itai-itai disease and health effects of cadmium. In: Chang, L.W. (Ed.), Toxicology of Metals. CRC Press, New York. Chen, M., Ma, L.Q., Singh, S.P., Cao, R.X., Melamed, R., 2003. Field demonstration of in situ immobilization of soil Pb using P amendment. Adv. Environ. Res. 8, 93 102. Chen, J., Qin, J., Zhu, Y.G., Lorenzo, V.D., Rosena, B.P., 2013. Engineering the Soil Bacterium Pseudomonas putida for Arsenic Methylation. Appl. Environ. Microbiol. 79, 4493 4495. Choudhary, M., Kumar, R., Datta, A., Nehra, V., Garg, N., 2017. Bioremediation of heavy metals by microbes. In: Arora, S., Singh, A.K., Singh, Y.P. (Eds.), Bioremediation of Salt Affected Soils: An Indian Perspective. Springer, Cham. Clarkson, T.W., 1993. Mercury: major issues in environmental health, Environ. Health Perspect., 100. pp. 31 38. Clarkson, T.W., 1997. The toxicology of mercury. Crit. Rev. Clin. Lab. Sci. 34, 369 403. Clarkson, T.W., Magos, L., 2006. The toxicology of mercury and its chemical compounds. Crit. Rev. Toxicol. 36, 609 662. Clarkson, T.W., Nordberg, G.F., Sager, P.R., 1983. Reproductive and Developmental Toxicity of Metals. Plenum Press, New York. Codd, R., Irwin, J.A., Lay, P.A., 2003. Sialoglycoprotein and carbohydrate complexes in chromium toxicity. Curr. Opin. Chem. Biol. 17, 213 219. Connell, D., 2005. Basic Concepts of Environmental Chemistry. CRC Press, Boca Raton, FL. Couillard, D., Zhu, S., 1992. Bacterial leaching of heavy metals from sewage sludge for agricultural application. Water Air Soil Pollut. 63, 67 80. Cullen, W.R., 2008. Is Arsenic an Aphrodisiac? The Sociochemistry of an Element. Royal Society of Chemistry, Cambridge, UK. Deng, D.M., Shu, W.S., Zhang, J., Zou, H.L., Ye, Z.H., Wong, M.H., et al., 2007. Zinc and cadmium accumulation and tolerance in populations of Sedum alfredii. Environ. Pollut. 147, 381 386. Dhankher, O.P., Li, Y., Rosen, B.P., Shi, J., Salt, D., Senecoff, J.F., et al., 2002. Engineering tolerance and hyper-accumulation of arsenic in plants by combining arsenate reductase and g-glutamylcysteine synthetase expression. Nat. Biotechnol. 20, 1140 1145. Dixit, R., Wasiullah, Malaviya, D., Pandiyan, K., Singh, U.B., Sahu, A., et al., 2015. Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7, 2189 2212. Duffus, J.H., 2002. “Heavy metals”- a meaningless term? Pure Appl. Chem. 74, 793 807. Dzairi, F.Z., Zeroual, Y., Moutaouakkil, A., Taoufik, J., Talbi, M., Loutfi, M., et al., 2004. Bacterial volatilization of mercury by immobilized bacteria in fixed and fluidized bed bioreactor. Ann. Microbiol. 54, 353 364. Eapen, S., D’Souza, S.F., 2005. Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol. Adv. 23, 97 114. El-Helow, E.R., Sabry, S.A., Amer, R.M., 2000. Cadmium biosorption by a cadmium resistant strain of Bacillus thuringiensis: regulation and optimization of cell surface affinity for metal cations. Biometals 13, 273 280. Fekih, B.I., Zhang, C., Li, Y.P., Zhao, Y., Alwathnani, H.A., Saquib, Q., et al., 2018. Distribution of arsenic resistance genes in prokaryotes. Front. Microbiol. 9, 1 11. Filipic, M., 2012. Mechanisms of cadmium induced genomic instability. Mut. Res. 733, 69 77.

Plant Life under Changing Environment

230

9. Genetic engineering approaches and applicability for the bioremediation of metalloids

Flathman, P.E., Lanza, G.R., 1998. Phytoremediation: current views on an emerging green technology. J. Soil Contam. 7, 415 432. Flora, S.J.S., 2002. Lead exposure: health effects, prevention and treatment. J. Environ. Biol. 23, 25 41. Flora, S.D., Bagnasco, M., Serra, D., Zanacchi, P., 1990. Genotoxicity of chromium compounds. A review. Mutat. Res. 238, 99 172. Francesconi, K., Visoottiviseth, P., Sridokchan, W., Goessler, W., 2002. Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: a potential phytoremediator of arsenic-contaminated soils. Sci. Total Environ. 284, 27 35. Francois, F., Lombard, C., Guigner, J.M., Soreau, P., Brian-Jaisson, M.G., Vandervennet, M., et al., 2012. Isolation and characterization of environmental bacteria capable of extracellular biosorption of mercury. Appl. Environ. Microbiol. 78, 1097 1106. Friberg, L., Piscator, M., Nordberg, G., 1971. The Itai-itai disease. In: Friberg, L., Piscator, M., Nordberg, G. (Eds.), Cadmium in the Environment. CRC Press, Ohio. Gadd, G.M., 2008. Transformation and mobilization of metals by microorganisms. In: Violante, A., Huang, P.M., Gadd, G.M. (Eds.), Biophysico-Chemical Processes of Heavy Metals and Metalloids in Soil Environments. Wiley, Chichester. Gadd, G.M., 2009. Heavy metal pollutants: environmental and biotechnological aspects. In: Schaechter, M. (Ed.), Encyclopedia of Microbiology. Elsevier, Oxford. Gadd, G.M., 2010. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156, 609 643. Garbisu, C., Hernandez-Allica, J., Barrutia, O., Alkorta, I., Becerril, J.M., 2002. Phytoremediation: a technology using green plants to remove contaminants from polluted areas. Rev. Environ. Health 17, 75 90. Gautam, P.K., Gautam, R.K., Banerjee, S., Chattopadhyaya, M.C., Pandey, J.D., 2016. Heavy metals in the environment: fate, transport, toxicity and remediation technologies. In: Pathania, D. (Ed.), Heavy Metals: Sources, Toxicity and Remediation Techniques. Nova Science Publishers, Inc. Ghosh, S., Mahapatra, N.R., Banerjee, P.C., 1997. Metal resistance in Acidocella strains and plasmid-mediated transfer of this characteristic to Acidiphilium multivorum and Escherichia coli. Appl. Environ. Microbiol. 63, 4523 4527. Gili, P., Medeiros, A., Lorenzo-Lorenzo-Louis, P.A., Rosa, E.M., Munoz, A., 2002. On the interaction of compounds of chromium(VI) with hydrogen peroxide. A study of chromium(VI) and (V) peroxides in the acidbasic pH range. Inorg. Chim. Acta 331, 16 24. Giller, K.E., Witter, E., McGrath, S.P., 1998. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils. Soil Biol. Biochem. 30, 1389 1414. Giri, A.K., Patel, R.K., Mahapatra, S.S., Mishra, P.C., 2013. Biosorption of arsenic(III) from aqueous solution by living cells of Bacillus cereus. Environ. Sci. Pollut. Res. 20, 1281 1291. Godt, J., Scheidig, F., Grosse-Siestrup, C., Esche, V., Brandenburg, P., Reich, A., et al., 2006. The toxicity of cadmium and resulting hazards for human health. J. Occup. Med. Toxicol. 1, 1 6. Guo, J., Dai, X., Xu, W., Ma, M., 2008. Over-expressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72, 1020 1026. Guo, S., Mahillon, J., 2013. pGIAK1, a heavy metal resistant plasmid from an obligate alkaliphilic and halotolerant bacterium isolated from the Antarctic Concordia Station confined environment. PLoS ONE 8, 1 8. Gupta, S., Nirwan, J., 2015. Evaluation of mercury biotransformation by heavy metal-tolerant Alcaligenes strain isolated from industrial sludge. Int. J. Environ. Sci. Technol. 12, 995 1002. Gupta, S., Goyal, R., Nirwan, J., Cameotra, S.S., Prakash, N.T., 2012. Biosequestration, transformation and volatilization of mercury by Lysinibacillus fusiformis isolated from industrial effluent. J. Microbiol. Biotechnol. 22, 684 689. Gupta, S., Goyal, R., Prakash, N.T., 2014. Biosequestration of lead using Bacillus strains isolated from seleniferous soils and sediments of Punjab. Environ. Sci. Pollut. Res. 21, 10186 10193. Haddad, J.K., Stenberg, E., 1963. Bronchitis due to acute mercury inhalation. Am. Rev. Respir. Dis. 88, 543 545. Halim, M., Conte, P., Piccolo, A., 2003. Potential availability of heavy metals to phytoextraction from contaminated soils induced by exogenous humic substances. Chemosphere 52, 265 275. Hawkes, J.S., 1997. What is a “Heavy metals”? J. Chem. Educ. 74, 1374.

Plant Life under Changing Environment

References

231

Heaton, A.C.P., Rugh, C.L., Wang, N.J., Meagher, R.B., 1998. Phytoremediation of mercury- and methylmercurypolluted soils using genetically engineered plants. J. Soil Contam. 7, 497 509. Hei, T.K., Liu, S.X., Waldren, C., 1998. Mutagenicity of arsenic in mammalian cells: role of reactive oxygen species. Proc. Natl. Acad. Sci. U.S.A. 95, 8103 8107. Hettick, B.E., Canas-Carrell, J.E., French, A.D., Klein, D.M., 2015. Arsenic: a review of the element’s toxicity, plant interactions, and potential methods of remediation. J. Agric. Food Chem. 63, 7097 7107. Housecroft, C.E., Sharpe, A.G., 2008. Inorganic Chemistry. Prentice Hall, Harlow. Hu, B., Cui, R., Li, J., Wei, H., Zhao, J., Bai, F., et al., 2013. Occurrence and distribution of heavy metals in surface sediments of the Changhua River Estuary and adjacent shelf (Hainan Island). Mar. Pollut. Bull. 76, 400 405. Huang, D., Zeng, G., Jiang, X., Feng, C., Yu, H., Huang, H., et al., 2006. Bioremediation of Pb-contaminated soil by incubating with Phanerochaete chrysosporium and straw. J. Hazard. Mater. 134, 268 276. Huang, K., Chen, C., Shen, Q., Rosen, B.P., Zhao, F.J., 2015. Genetically engineering Bacillus subtilis with a heatresistant arsenite methyltransferase for bioremediation of arsenic-contaminated organic waste. Appl. Environ. Microbiol. 81, 6718 6724. Hughes, M.F., Beck, B.D., Chen, Y., Lewis, A.S., Thomas, D.J., 2011. Arsenic exposure and toxicology: a historical perspective. Toxicol. Sci. 123, 305 332. IARC, 1993. Cadmium and certain cadmium compounds. IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Beryllium, Cadmium, Mercury and Exposures in the Glass Manufacturing Industry. IARC Monograph. World Health Organization. International Agency for Research on Cancer, Lyon, France, p. 58. Israr, M., Sahi, S., Datta, R., Sarkar, D., 2006. Bioaccumulation and physiological effects of mercury in Sesbania drummondii. Chemosphere 65, 591 598. Jain, C.K., 2004. Metal fractionation study on bed sediments of river Yamuna, India. Water Res. 38, 569 578. Jarup, H., 2003. Hazards of heavy metal contamination. Br. Med. Bull. 68, 167 182. Jarup, L., Berglund, M., Elinder, C.G., Nordberg, G., Vahter, M., 1998. Health effects of cadmium exposure—a review of the literature and a risk estimate. Scand. J. Work Environ. Health. 24, 1 51. Johnson, I., Flower, N., Loutit, M.W., 1981. Contribution of periphytic bacteria to the concentration of chromium in the crab Helice crassa. Microb. Ecol. 7, 245 252. Juwarkar, A.A., Nair, A., Dubey, K.V., Singh, S.K., Devotta, S., 2007. Biosurfactant technology for remediation of cadmium and lead contaminated soils. Chemosphere 68, 1996 2000. Kamal, M., Ghalya, A.E., Mahmouda, N., Cote, R., 2004. Phytoaccumulation of heavy metals by aquatic plants. Environ. Intern. 29, 1029 1039. Kim, S.K., Lee, B.S., Wilson, D.B., Kim, E.K., 2005. Selective cadmium accumulation using recombinant Escherichia coli. J. Biosci.Bioeng. 99, 109 114. Kramer, U., 2010. Metal hyperaccumulation in plants. Annu. Rev. Plant Biol. 61, 517 534. Kumar, P.S., Gunasundari, E., 2018. Bioremediation of heavy metals. In: Varjani, S., Agarwal, A., Gnansounou, E., Gurunathan, B. (Eds.), Bioremediation: Applications for Environmental Protection and Management. Energy, Environment and Sustainability. Springer, Singapore. Kumar, P.B.A.N., Dushenkov, V., Motto, H., Raskin, I., 1995. Phytoextraction: the use of plants to remove heavy metals from soils. Environ. Sci. Technol. 29, 1232 1238. Kumar, A., Cameotra, S.S., Gupta, S., 2012. Screening and characterization of potential cadmium biosorbent Alcaligenes strain from industrial effluent. J. Basic Microbiol. 52, 160 166. Kumar, N.M., Muthukumaran, C., Sharmila, G., Gurunathan, B., 2018. Genetically modified organisms and its impact on the enhancement of bioremediation. In: Varjani, S., Agarwal, A., Gnansounou, E., Gurunathan, B. (Eds.), Bioremediation: Applications for Environmental Protection and Management. Energy, Environment, and Sustainability. Springer, Singapore. Lakshmanasenthil, S., Vinothkumar, T., Ajith Kumar, T.T., Marudhupandi, T., Veettil, D.K., Ganeshamurthy, R., et al., 2013. Harmful metals concentration in sediments and fishes of biologically important estuary, Bay of Bengal. J. Environ. Health Sci. Eng. 11, 1 7. Langard, S., Vigander, T., 1983. Occurrence of lung cancer in workers producing chromium pigments. Br. J. Ind. Med. 40, 71 74.

Plant Life under Changing Environment

232

9. Genetic engineering approaches and applicability for the bioremediation of metalloids

Levinson, H.S., Mahler, I., 1998. Phosphatase activity and lead resistance in Citrobacter freundii and Staphylococcus aureus. FEMS Microbiol. Lett. 161, 135 138. Li, H., Cong, Y., Lin, J., Chang, Y., 2015. Enhanced tolerance and accumulation of heavy metal ions by engineered Escherichia coli expressing Pyrus calleryana phytochelatin synthase. J. Basic Microbiol. 55, 398 405. Liu, S., Zhang, F., Chen, J., Sun, G., 2011. Arsenic removal from contaminated soil via biovolatilization by genetically engineered bacteria under laboratory conditions. J. Environ. Sci. 23, 1544 1550. Lloyd, J.R., 2002. Bioremediation of metals: the application of microorganisms that make and break minerals. Microbiology 29, 67 69. Long, X.X., Yang, X.E., Ye, Z.Q., Ni, W.Z., Shi, W.Y., 2002. Differences of uptake and accumulation of zinc in four species of Sedum. Acta Bot. Sin. 44, 152 157. Long, D., Tang, X., Cai, K., Chen, G., Chen, L., Duan, D., et al., 2013. Cr(VI) reduction by a potent novel alkaliphilic halotolerant strain Pseudochrobactrum saccharolyticum LY10. J. Hazard. Mater. 257, 24 32. Lu, W.B., Shi, J.J., Wang, C.H., Chang, J.S., 2006. Biosorption of lead, copper and cadmium by an indigenous isolate Enterobacter sp. J1 possessing high heavy-metal resistance. J. Hazard Mater. B 134, 80 86. Ma, L.Q., Komar, K.M., Tu, C., Zhang, W.H., Cai, Y., Kennelley, E.D., 2001. A fern that hyperaccumulates arsenic a hardy, versatile, fast-growing plant helps to remove arsenic from contaminated soils. Nature 409, 579. Masih, D., Seida, Y., Izumi, Y., 2009. Arsenic removal from dilute solutions by high surface area mesoporous iron oxyhydroxide. Water Air Soil Pollut. 9, 203 211. Mazumder, D.N.G., 2000. Diagnosis and treatment of chronic arsenic poisoning. United Nations Synthesis Report on Arsenic in Drinking Water. WHO, Geneva, Switzerland. McGrath, S.P., Zhao, F.J., 2003. Phytoextraction of metals and metalloids from contaminated soils. Curr. Opin. Biotechnol. 14, 277 282. Menn, F.M., Easter, J.P., Sayler, G.S., 2000. Genetically engineered microorganisms and bioremediation. In: second ed Rehm, H.J., Reed, G. (Eds.), Biotechnology: Environmental Processes II, vol. 11b. Wiley, Germany. Mohammed, A.S., Kapri, A., Goel, R., 2011. Heavy metal pollution: source, impact, and remedies. In: Khan, M., Zaidi, A., Goel, R., Musarrat, J. (Eds.), Biomanagement of Metal-Contaminated Soils. Environmental Pollution, vol. 20. Springer, Dordrecht. Mokashi, S.A., Paknikar, K.M., 2002. Arsenic(III) oxidizing Microbacterium lacticum and its use in the treatment of arsenic contaminated groundwater. Lett. Appl. Microbiol. 34, 258 262. Monni, S., Salemma, M., Millar, N., 2000. The tolerance of Empetrum nigrum to copper and nickel. Environ. Pollut. 109, 221 229. Moore, J.N., Ficklin, W.H., Johns, C., 1988. Partitioning of arsenic and metals in reducing sulfidic sediments. Environ. Sci. Technol. 22, 432 437. Muchuweti, M., Birkett, J.W., Chinyanga, E., Zvauya, R., Scrimshaw, M.D., Lester, J.N., 2006. Heavy metal content of vegetables irrigated with mixture of wastewater and sewage sludge in Zimbabwe: implications for human health. Agr. Ecosyst. Environ. 112, 41 48. Mudhoo, A., Mohee, R., 2012. Elements of sustainability and bioremediation. In: Mohee, R., Mudhoo, A. (Eds.), Bioremediation and Sustainability. Scrivener, Wiley. Muller, U., 2007. Inorganic Structural Chemistry. Wiley, Chichester. Ndeda, L.A., Manohar, S., 2014. Determination of heavy metals in Nairobi Dam Water, (Kenya). IOSR J. Environ. Sci. Toxicol. Food Technol. 8, 68 73. Negri, M.C., Hinchman, R.R., 2000. The use of plants for the treatment of radionuclides. In: Raskin, I., Ensley, E. D. (Eds.), Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. Wiley, New York 7. Nies, D.H., 1992. Resistance to cadmium, cobalt, zinc, and nickel in microbes. Plasmid 27, 17 28. Nies, D.H., 1999. Microbial heavy-metal resistance. Appl. Microbiol. Biotechnol. 51, 730 750. Niu, H., Xu, X.S., Wang, J.H., Volesky, B., 1993. Removal of lead from aqueous solutions by Penicillium biomass. Biotechnol. Bioeng. 42, 785 787. Nongbri, B.B., Syiem, M.B., 2012. Analysis of heavy metal accumulation in water and fish (Cyprinus carpio) meat from Umiam lake in Meghalaya, India. Int. Multidis. Res. J. 2, 73 76. Nordberg, G., Jin, T., Bernard, A., Fierens, S., Buchet, J.P., Ye, T., et al., 2002. Low bone density and renal dysfunction following environmental cadmium exposure in China. Ambio 6, 478 481.

Plant Life under Changing Environment

References

233

O’Neil, M.J. (Ed.), 2003. The Merck Index. 15th ed. Merck & Co, Whitehouse Station, NJ. Osborn, A.M., Bruce, K.D., Strike, P., Ritchie, D.A., 1997. Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. FEMS Microbiol. Rev. 19, 239 262. Oves, M., Khan, S., Qari, H., Felemban, N., Almeelbi, T., 2016. Heavy metals: biological importance and detoxification strategies. J. Bioremed. Biodegrad. 7, 1 15. Oyetibo, G.O., Miyauchi, K., Suzuki, H., Endo, G., 2016. Mercury removal during growth of mercury tolerant and self-aggregating Yarrowia spp. AMB Exp. 6, 1 12. Papanikolaou, N.C., Hatzidaki, E.G., Belivanis, S., Tzanakakis, G.N., Tsatsakis, A.M., 2005. Lead toxicity update. A brief review. Med. Sci. Monitor 11, 329 336. Park, D., Yun, Y.S., Jo, J.H., Park, J.M., 2005. Mechanism of hexavalent chromium removal by dead fungal biomass of Aspergillus niger. Water Res. 39, 533 540. Patel, P.C., Goulhen, F., Boothman, C., Gault, A.G., Charnock, J.M., Kalia, K., et al., 2007. Arsenate detoxification in a Pseudomonad hypertolerant to arsenic. Arch. Microbiol. 187, 171 183. Patra, M., Sharma, A., 2000. Mercury toxicity in plants. Bot. Rev. 66, 379 422. Patra, M., Bhowmik, N., Bandopadhyay, B., Sharma, A., 2004. Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ. Exp. Bot. 52, 199 223. Pirkle, J.L., Kaufmann, R.B., Brody, D.J., Hickman, T., Gunter, E.W., Paschal, D.C., 1998. Exposure of the U.S. population to lead: 1991 1994. Environ. Health Perspect. 106, 745 750. Qin, J., Rosen, B.P., Zhang, Y., Wang, G., Franke, S., Rensing, C., 2006. Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc. Natl. Acad. Sci. U.S. A. 103, 2075 2080. Reddy, A.M., Kumar, S.G., Jyotsnakumari, G., Thimmanayak, S., Sudhakar, C., 2005. Lead induced changes in antioxidant metabolism of horse gram (Macrotyloma uniflorum (Lam.) Verdc.) and Bengal gram (Cicer arietinum L.). Chemosphere 60, 97 104. Reeves, R.D., Baker, A.J.M., 2000. Metal-accumulating plants. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. Wiley, New York. Rehman, K., Fatima, F., Waheed, I., Akash, M.S.H., 2017. Prevalence of exposure of heavy metals and their impact on health consequences. J. Cell. Biochem. 119, 157 184. Rensing, C., Sun, Y., Mitra, B., Rosen, B.P., 1998. Pb(II)-translocating P-type ATPases. J. Biol. Chem. 273, 32614 32617. Roane, T.M., Josephson, K.L., Pepper, I.L., 2001. Dual-bioaugmentation strategy to enhance remediation of cocontaminated soil. Appl. Environ. Microbiol. 67, 3208 3215. Roane, T.M., Pepper, I.L., Gentry, T.J., 2014. Microorganisms and metal pollutants, Environmental Microbiology, third ed. Elsevier Inc. Rojas, L.A., Yanez, C., Gonzalez, M., Lobos, S., Smalla, K., Seeger, M., 2011. Characterization of the metabolically modified heavy metal-resistant Cupriavidus metallidurans strain MSR33 generated for mercury bioremediation. PLoS ONE 6, 1 10. Rosen, B.P., 2002. Biochemistry of arsenic detoxification. FEBS Lett. 529, 86 92. Rossman, T.G., 2003. Mechanisms of arsenic carcinogenesis. An integrated approach. Mutat. Res. 533, 37 65. Rugh, C.L., Senecoff, J.F., Meagher, R.B., Merkle, S.A., 1998. Development of transgenic yellow poplar for mercury phytoremediation. Nat. Biotechnol. 16, 925 928. Saha, B., Orvig, C., 2010. Biosorbents for hexavalent chromium elimination from industrial and municipal effluents. Coord. Chem. Rev. 254, 2959 2972. Sakai, H., Kojima, Y., Saito, K., 1986. Distribution of metals in water and sieved sediments in the Toyohira River. Water Res. 20, 559 567. Salt, D.E., Blaylock, M., Kumar, N.P.B.A., Viatcheslav, D., Ensley, B.D., Chet, I., et al., 1995. Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Bio-Technology 13, 468 474. Salt, D.E., Smith, R.D., Raskin, I., 1998. Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 643 668. Sardrood, B.P., Goltapeh, E.M., Varma, A., 2013. An introduction to bioremediation. In: Goltapeh, E., Danesh, Y., Varma, A. (Eds.), Fungi as Bioremediators. Soil Biology, vol. 32. Springer, Berlin, Heidelberg.

Plant Life under Changing Environment

234

9. Genetic engineering approaches and applicability for the bioremediation of metalloids

Satarug, S., Moore, M.R., 2004. Adverse health effects of chronic exposure to low-level cadmium in foodstuffs and cigarette smoke. Environ. Health Perspect. 112, 1099 1103. Seaward, M.R.D., Richardson, D.H.S., 1990. Atmospheric sources of metal pollution and effects on vegetation. In: Shaw, A.J. (Ed.), Heavy Metal Tolerance in Plants Evolutionary Aspects. CRC Press, Boca Raton, FL. Seidal, K., Jorgensen, N., Elinder, C.G., Sjogren, B., Vahter, M., 1993. Fatal cadmium-induced pneumonitis. Scand. J. Work Environ. Health. 19, 429 431. Selvin, J., Shanmugha, P.S., Seghal, K.G., Thangavelu, T., Sapna, B.N., 2009. Sponge-associated marine bacteria as indicators of heavy metal pollution. Microbiol. Res. 164, 352 363. Shelnutt, S.R., Goad, P., Belsito, D.V., 2007. Dermatological toxicity of hexavalent chromium. Crit Rev. Toxicol. 37, 375 387. Shen, H., Wang, Y.T., 1993. Characterization of enzymatic reduction of hexavalent chromium by Escherichia coli ATCC 33456. Appl. Environ. Microbiol. 59, 3771 3777. Silver, S., Phung, L.T., 1996. Bacterial heavy metal resistance: new surprises. Annu. Rev. Microbiol. 50, 753 789. Silver, S., Phung, L.T., 2005. A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J. Ind. Microbiol. Biotechnol. 32, 587 605. Singh, B.R., McLaughlin, M.J., 1999. Cadmium in soils and plants. In: McLaughlin, M.J., Singh, B.R. (Eds.), Developments in Plant and Soil Sciences, vol. 85. Kluwer Academic Publishers, Dordrecht. Smedley, P.L., Kinniburgh, D.G., 2002. A review of the source, behaviour and distribution of arsenic in natural waters. Appl. Geochem. 17, 517 568. Smith, L.A., Means, J.L., Chen, A., Alleman, B., Chapman, C.C., Tixier, J.S., et al., 1995. Remedial Options for Metals-Contaminated Sites. Lewis Publishers, Boca Raton, FL. Song, W.Y., Sohn, E.J., Martinoia, E., Lee, Y.J., Yang, Y.Y., Jasinski, M., et al., 2003. Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat. Biotechnol. 21, 914 919. Stiborova, M., Pitrichova, M., Brezinova, A., 1987. Effect of heavy metal ions in growth and biochemical characteristic of photosynthesis of barley and maize seedlings. Biol. Plant 29, 453 467. Sudhakar, G., Jyothi, B., Venkateswarlu, V., 1991. Metal pollution and its impact on algae in flowing waters in India. Arch. Environ. Contam. Toxicol. 21, 556 566. Summers, A.O., 1986. Organization, expression and evolution of genes for mercury resistance. Annu. Rev. Microbiol. 40, 607 634. Tchounwou, P.B., Yedjou, C.G., Patlolla, A.K., Sutton, D.J., 2012. Heavy metal toxicity and the environment, Molecular, Clinical and Environmental Toxicology. Experientia Supplementum, vol 101. Springer, Basel. Tripathi, R.D., Srivastava, S., Mishra, S., Singh, N., Tuli, R., Gupta, D.K., et al., 2007. Arsenic hazards: strategies for tolerance and remediation by plants. Trend Biotechnol. 25, 158 165. Turpeinen, R., Kallio, M.P., Kairesalo, T., 2002. Role of microbes in controlling the speciation of arsenic and production of arsines in contaminated soils. Sci. Total Environ. 285, 133 145. Vidali, M., 2001. Bioremediation. An overview. Pure Appl. Chem. 73, 1163 1172. Wang, J., Chen, C., 2006. Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol. Adv. 24, 427 451. Wang, C.L., Michels, P.C., Dawson, S.C., Kitisakkul, S., Baross, J.A., Keasling, J.D., et al., 1997. Cadmium removal by a new strain of Pseudomonas aeruginosa in aerobic culture. Appl. Environ. Microbiol. 63, 4075 4078. Wang, J., Zhao, F.J., Meharg, A.A., Raab, A., Feldmann, J., McGrath, S.P., 2002. Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol. 130, 1552 1561. Weiss, B., Clarkson, T.W., Simon, W., 2002. Silent latency periods in methylmercury poisoning and in neurodegenerative disease. Environ. Health Perspect. 110, 851 856. WHO, 2001. Arsenic and arsenic compounds, Environmental Health Criteria, vol. 224. World Health Organization, Geneva. WHO, 2003. Elemental Mercury and Inorganic Mercury Compounds: Human Health Aspects. World Health Organization, Geneva. WHO, 2011. Evaluation of Certain Food Additives and Contaminants: Seventy-Third Report of the Joint FAO/ WHO Expert Committee on Food Additives. WHO Technical Report Series. Wilson, D.N., 1988. Cadmium—market trends and influences. In: Cadmium 87. Proceedings of the Sixth International Cadmium Conference, London.

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Further reading

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Wintz, H., Fox, T., Vulpe, C., 2002. Responses of plants to iron, zinc and copper deficiencies. Biochem. Soc. Trans. 30, 766 768. Wong, P.T.S., Chau, Y.K., Luxon, P.L., 1975. Methylation of lead in the environment. Nature 253, 263 264. Wuana, R.A., Okieimen, F.E., 2011. Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol. 2011, 1 20. Yan, G., Viraraghavan, T., 2001. Heavy metal removal in biosorption column by Mucor rouxii biomass. Bioresour. Technol. 78, 243 249. Yong, X., Chen, Y., Liu, W., Xu, L., Zhou, J., Wang, S., et al., 2014. Enhanced cadmium resistance and accumulation in Pseudomonas putida KT2440 expressing the phytochelatin synthase gene of Schizosaccharomyces pombe. Lett. Appl. Microbiol. 58, 255 261. Yuan, C.G., Lu, X.F., Qin, J., Rosen, B.P., Li, X.C., 2008. Volatile arsenic species released from Escherichia coli expressing the AsIII S-adenosylmethionine methyltransferase gene. Environ. Sci. Technol. 42, 3201 3206. Zeroual, Y., Moutaouakkil, A., Blaghen, M., 2001. Volatilization of mercury by immobilized bacteria (Klebsiella pneumoniae) in different support by using fluidized bed bioreactor. Curr. Microbiol. 43, 322 327. Zeyaullah, M., Haque, S., Nabi, G., Nand, K.N., Ali, A., 2010. Molecular cloning and expression of bacterial mercuric reductase gene. Afr. J. Biotechnol. 9, 3714 3718. Zhang, Z., Yin, N., Cai, X., Wang, Z., Cui, Y., 2016. Arsenic redox transformation by Pseudomonas sp. HN-2 isolated from arsenic-contaminated soil in Hunan, China. J. Environ. Sci. (China) 47, 165 173. Zhao, F.J., Dunham, S.J., McGrath, S.P., 2002. Arsenic hyperaccumulation by different fern species. New Phytol. 156, 27 31. Zhou, Z.S., Huang, S.Q., Guo, K., Mehta, S.K., Zhang, P.C., Yang, Z.M., 2007. Metabolic adaptations to mercuryinduced oxidative stress in roots of Medicago sativa L. J. Inorg. Biochem. 101, 1 9. Zhu, Y.L., Pilon-Smits, E.A.H., Jouanin, L., Terry, N., 1999a. Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 119, 73 79. Zhu, Y.L., Pilon-Smits, E.A.H., Tarun, A.S., Weber, S.U., Jouanin, L., Terry, N., 1999b. Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol. 121, 1169 1177.

Further reading Meagher, R.B., Rugh, C.L., Kandasamy, M.K., Gragson, G., Wang, N.J., 2000. Engineered phytoremediation of mercury pollution in soil and water using bacterial genes. In: Terry, N., Bauelos, G. (Eds.), Phytoremediation of Contaminated Soil and Water. Lewis Publishers, Boca Raton, FL. Wasi, S., Tabrez, S., Ahmad, M., 2013. Use of Pseudomonas spp. for the bioremediation of environmental pollutants: a review. Environ. Monit. Assess. 185, 8147 8155.

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10 Responses of plants to herbicides: Recent advances and future prospectives Suruchi Singh and Supriya Tiwari Department of Botany, Institute of Science, Banaras Hindu University, Varanasi, India

10.1 Introduction Multitude factors have led to increased use of pesticides in recent times. Growing risk of pests, diseases and weeds can also be attributed to environmental and agroecosystem disturbances. The high toxicity of currently available pesticides imposes environmental and health risks, and growing resistance and cross resistance of pests, herbs and insects to existing pesticides which complicates the situation. To cope, farmers adopted two strategies, first, they added fertilizers for favoring plant growth and second, protecting crops from pathogens attacks and competition with weeds. All these biotic stresses cause damages to crops resulting in severe yield losses and/or a decrease of yield quality. At present, use of agrochemicals is the main strategy to counteract these issues. Agrochemicals are divided into several classes depending on their specific target organisms. Herbicides, insecticides, and fungicides are the most widely used chemicals, comprising 47%, 29%, and 18% of the total chemicals used respectively and representing an annual turnover of 30,000 million euros (Bonnemain and Chollet, 2002). Most of the commercialized agrochemicals have toxicological and ecotoxicological side effects. However, despite their ability to have impacts on target organisms, they have additional ability to generate nonspecific toxicity. In the environment, pesticide residues from cultivable fields are released in soil and water (Mansour, 2004; PapadopoulousMourkidou et al., 2004). Regarding human health, pesticides create issues not only for farmers who are in contact with the active molecules but also for consumers due to transformed forms of pesticide residues from agriculture (Weichenthal et al., 2010). Out of the total applied amount of pesticides, only a small fraction (,0.1%) reaches the target sites (Pimental, 1995). Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00011-4

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Chemical pesticides displayed potential by enhancing agricultural productivity at global scale, thereby reducing recurrence of diseases and thus contributing both in protection and restoration of vegetation of all types. The usages of pesticides are more in developing countries particularly those lying in the tropical regions and by supplying off-season fruits and vegetables to temperate countries are participating in the global economy. The stats for the global sales revealed that, among all other pesticides, herbicides are most widely applied. Even if a certain active ingredients is selective to the crop and does not cause many injuries to the plants, biochemical and physiological alterations may occur (Song et al., 2007a,b). Developed nations have now focused on using natural products as herbicides (Table 10.1) (Dayan et al., 2009). In this chapter, we have discussed the direct and indirect effect of herbicides on physiology of plants.

10.2 Phenotypical manifestation Visible symptoms are frequently used to evaluate the effects of pesticide treatments on crops. Damages are more common following herbicide treatments than insecticide or fungicide treatments mainly because of the specific physiological targets. For example, diphenyl ether herbicide acifluorfen used on crops, such as soybean, bean, pea, broad bean, celery, cotton and spinach damaged leaves. Injury increases with the total amount of pesticide applied, and young, actively growing leaves are more susceptible to injury. Symptoms of pesticide injury are similar for all chemical types. Affected leaves become thickened and become hard and brittle. Leaves may appear smaller than normal and may be even distorted. Both foliage and fruit may appear bronzed or burned. Chlorotic and necrotic areas develop on leaves followed by desiccation and wilting. In cotton, additional symptoms were recorded such as red-brown spots on leaf veins (Berger et al., 2012). Herbicide residues may persist in soils at phytotoxic concentration and cause injuries on the crop species that is cultivated thereafter. Visible injuries are rarely observed after fungicide and insecticide treatments. However, it was reported that organophosphate, used on celery, caused the development of brown and dry areas or sunken lesions on the lower portion of petioles. The visible symptoms are not always the best approach to assess the effect of pesticide on crops. Indeed these injuries are difficult to quantify because of the broad symptom variations. Moreover, visible damages are difficult to correlate with a loss of yield since the perturbations of plant physiology leading to a yield reduction may also occur even if visible symptoms are not observed.

10.3 Herbicides: a multifaceted chemical There are multitudes of impacts of herbicides on plants (Fig. 10.1). There are several pathways through which the physiological processes are affected by herbicides. Herbicides have specific affinities for the target sites in vital plant biochemical pathways and/or physiological processes (Dayan et al., 2010; Falk et al., 2006) (Fig. 10.2).

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TABLE 10.1

List of natural products used as herbicides.

Herbicide

Features

Targets

Reference(s)

Corn gluten meal

• • • • • • •

• Effective for the young weeds

Quarles (1999)

Acetic acid

Fatty acids

Ineffective against existing weeds Cost prohibitive Can replace glyphosate Does not harm soil microorganism Does not control underground parts Can replace imazapyr and glyphosate Fatty acids of various aliphatic length mixed with vinegar or acetic acid and emulsifiers.

Essential oils • Pine oil • Clove oil

• 2-Phenethyl propionate

• Composed of terpene alcohols and saponified fatty acids • Steam distillation of clove leaves contains primarily eugenol in addition to other terpenoids • Matran contains up to 50% clove oil and Burnout II consists of a mixture of 12% clove oil with acetic acid

• Used in noncropland areas Young (2004) • For controlling annual weeds, mosses and liverwort • Nonselective contact herbicide (burn down)

• Clove oil is also been formulated for the control of poison ivy (Rhus radicans L.) • At low concentration controlled small weed but relatively high rate required for control

• A component of peppermint, which is also rich in menthol and menthone

Allelopathy • Momilactone-B • Sorgoleone Benzoxazinoids • •

Scarfato et al. (2007) Young (2004)

• Lemongrass oil • Obtained from Cymbopogon citratus Stapf or Cymbopogon flexuosus • 80% of this oil is citral • Citronella oil • Obtained from many plants mainly from Cymbopogon • Primary components are citronellal (42%), geraniol (21%) and other terpenes • Bialaphos • Tripeptide obtained from the fermentation culture of the actinomycetes Streptomyces hygroscopicus

• • • •

Malkomes (2006)

• It is a proherbicide that is metabolized into the active ingredient Lphosphinothricin in the treated plant • Bialaphos and phosphinothricin inhibit glutamine synthase Plays a key role in rice allelopathy • Inhibit the germination A lipid benzoquinone that exudes from and growth of neighboring the roots of Sorghum weeds Isolated from many species within the • Suppresses the growth of a Poaceae family large number of plant These glycosides are subjected to species microbial degradation when released into the environment, which released the aglycone moieties

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Dayan et al. (2009)

Bouverat-Bernier and Gallotte (1992) Charlesworth (1924) Clay et al. (2005)

Lydon and Duke (1999)

Hoy and Stickey (1881)

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Herbicide: mode of action Application

Cytological

Damaged tissue

Physiological

Bio-chemical Sensitive growth phase

Sensitive cell type: meristematic or elongating

Cellular or subcellular

In vivo inhibition of metabolic pathway

In vivo inhibition of metabolic pathway

Protein/ Enzyme interact ion

Sensitive enzymatic reaction and/or binding protein

FIGURE 10.1

Different modes of action of herbicides in plants.

P680*

P700* Pheophytin Ferredoxin QA

3

NADP+ reductases

QB Plastoquinone pool

NADP+

Cytochrome Fe-S protein

NADPH

4

2 Plastocyanin PSII 2H2O

1

PSI

O2+4H+

S-states

FIGURE 10.2 Site of action of herbicides on different targets of light reaction (1) phenolics on S-states, (2 and 3) triazine, triazinone, uracil, phenylcarbamate, triazolinone, pyridazinone, urea, amide, nitrile, phenylpyridazine and benzothiadiazinone on PSII, and (4) bipyridilium on PSI. PS, Photosystem.

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10.4 Physiological damage through generated reactive oxygen species intermediates One of the important consequences of herbicide application in agricultural system is the ´ generation of oxidative stress in plants (Jabłonska-Trypuc, 2017; Lukatkin et al., 2013; Chen et al., 2012). A quick rise in the level of reactive oxygen species (ROS) causes a common response of oxidative burst in plants against herbicide treatment. Common ROS generated in response to herbicide treatment are superoxide anion (O2 2 ), hydroxyl radical (OH), singlet oxygen (1O2), and hydrogen peroxide (H2O2). Oxidative stress induced by herbicides oxyfluorfen (Langaro et al., 2017), norflurazon (Jung, 2003), anthracene (Ivanov et al., 2005), clethodium (Radwan, 2012), and lactofen (Ferreira et al., 2010) have been well studied. The mode of action of herbicides varied substantially and still it is not clear whether all herbicides should act as prooxidants. It has been observed that the plant responses to herbicides are very selective (Dayan and Watson, 2011). A herbicide paraquat (methyl viologen) causes oxidative stress and suppresses antioxidant defense and also induce ultrastructural changes (Yoon et al., 2011). ROS are majorly produced in plants by photosynthesis, photorespiration, respiration, NAPPH oxidases, xanthane oxidases, oxidases and peroxidase (Apel and Hirt, 2004). The use of herbicides can generate stress conditions even in tolerant cultivars. However, the differential selectivity between species and degree of tolerance or susceptibility to herbicides is determined by the genetic makeup of species or cultivars. During herbicide treatment, chloroplasts play an important role in ROS production. The photosystem I (PSI) and photosystem II (PSII) reaction centers posses an oxygen-rich environment which is a favorable condition for ROS generation. Herbicides inhibiting photosynthesis can be categorized into two broad groups: PSII and PSI inhibitors. Herbicides belonging to both these groups block the synthesis of adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide phosphate hydrogen (NADPH), which is succeeded by ROS production and thus oxidative damage. Common bipyridinium herbicides, namely, paraquat and diquat act as an inhibitor of photosynthesis and exercise their herbicidal influence by acting as the ultimate electron acceptor of PSI thus replacing NADP1 (Chen et al., 2012). Upon being exposed to sunlight, the herbicides instead accept electrons from PSI and 2 leads to the generation of superoxide anions (O2 2 ) by passing e (s) to oxygen and further • forms H2O2 and OH (Fo¨rster et al., 2005). There are many other herbicides that display their toxicity mechanisms by ROS generation by blocking the photosynthetic electron chain, thus contributing in oxidative stress generation (Abdollahi et al., 2004). Chen et al. (2012) observed that Arabidopsis thaliana leaves on being treated with 3-AIPTA showed inhibitory effects on PSII electron transport beyond QA. Similarly, Bentazon effects photosynthesis by blocking the QB site of D1 protein present on the PSII complex (Nohatto et al., 2016). Herbicides, such as diuron, atrazine, bentazon, bromoxynil, metribuzin and hexazinone, also target the PSII, thus resulting in chloroplastic oxidative burst (Nohatto et al., 2016). Excess ROS generation in electron transport chain due to herbicide treatment destroy the cell membrane integrity and damages membrane, thus causing leakage and cellular destruction and lead to plant necrosis (Chen et al., 2012). Another herbicide, diphenyl ether targets the membrane system of thylakoids (Etemadi-Aleagha et al., 2002). Varshney et al. (2012) reported that the use of isoproturon affected the ultrastructure of

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photosynthetic apparatus of wheat and decreased the activity of ribulose bisphosphate carboxylase. Oxyfluorfen is an inhibitor of protoporphyrinogen oxidase (PROTON), which is an enzyme bounded to the inner membrane of chloroplast and catalyzes oxidation of protoporphyrinogen IX into protoporphyrin IX by establishing a conjugated system of double bonds and directly affects the chlorophyll synthesis route. The protoporphyrin IX interacts with molecular oxygen and light forming 1O2 which in turn triggers the oxidative processes (Tripathy et al., 2007). Herbicides not only act as inhibitors of photosynthesis and electron transport chain but also disrupt other metabolic processes of the plants. Penoxsulam functions as an inhibitor of acetolactate synthase (ALS), while imazamox inhibits the synthesis of acetohydroxyacid which disrupts the biosynthesis of amino acids leucine, isoleucine, and valine (Gettys and Haller, 2009). Disruption in the biosynthesis of these amino acids hampers the process of protein synthesis, which negatively affects the cell-division process (Oliveira Junior et al., 2011). Rimsulfuron, iodosulfuron, and metsulfuron also belong to the group of ALS inhibitor herbicides. Cyhalofop-butyl, haloxyfop-methyl, and clethodim restrict acetyl Co-A carboxylase, thus checking the plant’s ability to produce malonyl Co-A needed for the synthesis of fatty acids (Ruiz-Santaella et al., 2006). Deficiency of fatty acids is responsible for the abnormality in cell permeability and also disintegrates the structure of cell membranes (Oliveira Junior et al., 2011).

10.4.1 Protein oxidation Herbicides, especially those belonging to the group dithiocarbamates, are associated with the adverse effects on protein structure of the plants which is evident through the observed increase in the concentration of protein carbonyl groups (Astiz et al., 2009). Herbicide-induced modification in protein structure results in the accumulation of modified proteins in the cells which may trigger off programmed cell death, depending upon the protein targeted by the herbicide action (Grune and Davies, 2003). Furthermore, ROS generated oxidative stress brings about oxidation of cellular thiol groups which are dimerized to form disulfides. Oxidative damage to thiol groups causes a rapid loss of biological activities of proteins, which subsequently leads to significant dysfunction of a number of transporters and enzymes and the disruption of calcium homeostasis of the cell ´ (Jabłonska-Trypuc, 2017). Studies have shown that protein oxidation in herbicide-treated plants not only bring about changes in membrane permeability but also leads to the reduction of cytochrome c and metal ions (Dalle-Donne et al., 2006). Kumar (2012) showed that the protein contents in three varieties of wheat (HUW 234, HUW 468, and HUW 533) decreased significantly upon treatment with different levels of 2,4-dichlorophenoxy acetic acid (2,4-D) and isoproturon.

10.4.2 Lipid peroxidation Lipid peroxidation also acts as important oxidative markers in addition to ROS generation in herbicide-treated plants (Langaro et al., 2017; Nohatto et al., 2016; Lukatkin et al., 2013). ´ Jabłonska-Trypuc (2017), after reviewing a number of herbicides, observed that herbicides

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belonging to the group dithiocarbamates specifically targeted the membrane lipids. Herbicide-treated plants showed an elevated concentration of thiobarbituric acid reactive compounds, which is an indicator of increased lipid peroxidation. Enhanced lipid peroxidation causes cytoplasmic and mitochondrial membrane damage and depolarization resulting in an increased production of free oxygen radicals within the cell (Varshney et al., 2012). In addition to increased lipid peroxidation, certain herbicides also inhibit biosynthesis of lipids. Lukatkin et al. (2013) studied the effects of TOPIK, which is a aryloxyphenoxypropionate class of herbicide on wheat (cultivar Mironovskaya 808), winter rhy (Secale cereale L. cultivar Estafeta Tatarstana) and maize (Zea mays L cultivar Kollektivnyi 172 MV). The TOPIK herbicide checks the growth of both the mono- and dicotyledonous plants and is desirable for cereal stands. Although the main mode of action of TOPIK is to restrict lipid biosynthesis, the oxidative stress produced by the action of this herbicide in plants led to the peroxidation of lipid component of membrane, which is measured in terms of malondialdehyde (MDA) concentration in the plants (Lukatkin et al., 2013). It was observed that highest accumulation of MDA was in wheat (which was approximately 90% higher than the control one), whereas the percentage respective increase in maize and rye were 35% and 45% compared to water control (Lukatkin et al., 2013).

10.4.3 Antioxidant defense in response to herbicide treatment In response to the herbicide-induced oxidative stress, plants have developed an antioxidant system which scavenges the excess ROS generated in plants treated with herbicides (Langaro et al., 2017, 2016). The different enzymatic [superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), etc.] and nonenzymatic (phenolic compounds, ascorbic acid, glutathione, carotenoids, proline, etc.) components of the antioxidant system act in a sequential manner to eliminate the ROS necessary to resist herbicide-induced oxidative stress (Gill and Tuteja, 2010). Langaro et al. (2016) studied the response of different antioxidant enzymes in rice plants, 24 hours after the herbicide treatment, and found that SOD and CAT activity did not show any significant increase in the case of any of the seven herbicide treatments. However, SOD activity increased significantly at 120 hours after herbicide application in the case of plants treated with quinelorac, cyhalofop-butyl, and carfentrazoneethyl (Langaro et al., 2016). Agostinetto et al. (2016) also recorded similar observations in SOD activity, which did not show any significant increase at initial stage of sampling (24 hours after spraying) but increased significantly at 120 hours after spraying in wheat treated with clodinafop, metsulfuron, and 2,4-D. These observations suggest that in the case of rice, 24 hours may not be sufficient to activate the defense system. In another study, an increase of 243% in the SOD activity was recorded when the plants were treated with atrazine (Zhang et al., 2014). High SOD activity was also recorded in rice plants treated with bentazon and penoxsulam as compared to control (Nohatto et al., 2016). In wheat, increased SOD activity was recorded upon treatment with haloxyfop-methyl (Janicka et al., 2008). Contrary to these results, reduced SOD activity was observed in maize after clethodim application (Radwan, 2012). Although the reason for this variability is not known, it is presumed that the response of plants to herbicides depends upon the species sensitivity as well as the on enzyme isoform (Nohatto et al., 2016).

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Langaro et al. (2016) recorded an increase in CAT activity in rice upon treatment with bentazon, probably due to rapid accumulation of H2O2. However, Nohatto et al. (2016) observed lower CAT activity in rice upon treatment with bentazon and penoxsulam, as compared to control. CAT enzyme inhibition was also recorded in rice treated with oxyfluorfen (Langaro et al., 2017) and wheat treated with chlorotoluron (Song et al., 2007a,b). Reduction in CAT activity was accompanied by increase in H2O2 concentration after the bentazon and penoxsulam applications (Nohatto et al., 2016). This suggests that the reduction in CAT activity can be attributed to either in enzyme synthesis inhibition or due to variation in enzyme subunits assemblage under the stress generated by bentazon and penoxsulam (Abedi and Pakniyat, 2010). However, the reduced accumulation of H2O2 in wheat treated with bentazon and 2,4-D is attributed to higher CAT activity (Agostinetto et al., 2016). Results obtained by Nohatto et al. (2016) suggest that bentazon and penoxsulam had a higher potential of generating oxidative stress in rice than cyhalofop-butyl. APX is an important enzyme of the antioxidant defense system of plants due to its higher affinity for H2O2 when compared to CAT, even when H2O2 is present in low concentration (Gill and Tuteja, 2010). APX activity did not show any significant variation in rice plants treated with different groups of herbicides (Langaro et al., 2016). However, a higher activity of APX in rice plants treated with oxadiazon and pendimethalin has been verified by Langaro et al. (2017). Rice plants on being treated with inhibitors of PROTOX from various chemical groups (acifluorfem, oxyfluorfen, carfentrazone-ethyl and oxadiazon) displayed an increase in APX activity (of 68%), compared to control plants (Jung et al., 2008). Song et al. (2007a,b) also recorded an increase in APX activity in both leaves and roots of wheat subjected to application of chlorotoluron. Proline, which is an important nonenzymatic component of the antioxidant system in plants, increased in rice plants upon the application of oxyfluorfen (Langaro et al., 2017). It is believed that this increase is due to the role played by proline against oxidative damage due to the ability to eliminate ROS from the cell (Molinari et al., 2007). Proline accumulation can be attributed either to the increase of protein hydrolysis under stress or because of the conversion of sugars in the glutamate pathway. This is because proline acts as a mediator of osmotic adjustment, and on integrity and protection of the plasma membrane, it acts as a source of carbon and nitrogen and as an antioxidant agent, removing ROS during oxidative stress (Hemaprabha et al., 2013). Lukatkin et al. (2013) observed that the total antioxidant activity of wheat, rye, and maize increased by 2.1 5.8 times after 3 hours of application of TOPIK, which depicts the activation of the antioxidant defense system in these plants upon herbicide application.

10.5 Direct damage to the physiological process Photosynthesis is the biological phenomenon of transforming light to chemical energy and occurs in two major phases, that is, the light reaction (Hill reaction) and the dark reaction (Calvin cycle). Herbicides inhibit physiological processes through different ways, although no inhibiting action of herbicide on Calvin cycle has been developed.

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10.5.1 Photosystem II inhibitor Light reaction involves e2 transports which have potential to produce reactive and damaging intermediates which can form ROS. This is the reason why these processes are confined to the spaces enclosed by lipid bilayers. The light reaction of photosynthesis occurs within the thylakoid membranes of the chloroplasts where splitting of water is catalyzed by light, and the reaction releases O2 and is the source of e2 required for CO2 assimilation into the chemical energy. Photosynthesis utilizes light for energizing e2, which generates ROS that can damage the photosynthetic apparatus. Intricate antioxidative system neutralizes these ROS or converts them in lesser toxic forms (Mittler, 2002). However, herbicides restrain these protective processes by constraining the flow of e2 by complexing with the binding site of plastoquinone of PSII. Also, no other PSII inhibitors known cause any notably significant electrolyte leakage. Some herbicides, for instance, urea, triazines, and phenolic herbicides block the exchangeable quinone (QB) site present on D1; this protein subunit constitutes half fraction of the heterodimeric reaction center of PSII (Bowyer, 1991; Hock et al., 1995). This is the way, these herbicides prevents photosynthetic e2 flow further beyond one e2 reduction of quinone, QA (Bowyer, 1991; Hock et al., 1995). On the other hand, phenolic herbicides functions as uncouplers of the bioenergetic membrane reaction and fasten the decomposition of the S-states of the O2-evolving complex (Bowyer, 1991; Hock et al., 1995). Binding of herbicides to the QB site of the D1 protein can lead to photodamage of PSII in two ways: (1) they hamper photochemical reaction and (2) bind to the D1 protein and accelerate protein degradation.

10.5.2 Photosystem I inhibitors PSI is an assembly of more than 10 Psa proteins; the core of this complex being formed by PsaA and PsaB proteins. Movement of electrons from plastoquinone to plastocyanin is received by four redox factors that is present in the core of protein complex of PSI. Two iron sulfur congregate sited within PsaC carries e2 to ferredoxin (Brettel, 1997; Chitnis, 1996). The communication between common bipyridylium herbicides such as paraquat and diquat, and PSI is predicted to happen near the PsaC protein, where these compounds sidetrack e2(s) from the regular photosynthetic course. The mode of action of bipyridylium herbicides is different from other PSII inhibitors, while other herbicides restrict the e2 transfer by competing for the binding sites of plastoquinone. Bipyridylium herbicides prevent NADP reduction by diverting e2(s) from PSI (Hess, 2000; Trebst, 2007). Also, bipyridylium is capable of causing more severe phytotoxic symptoms than PSII inhibitors.

10.5.3 Amino acid biosynthesis Herbicides, which inhibit ALS, belong to structurally diverse five chemical classes: sulfonylureas, imidazolinones, triazolopyrimidines, pyrimidinylthio(or oxy)-benzoates and sulfonylamino-carbonyltriazolinones (Zhou et al., 2007). This enzyme facilitates the condensation of 2 3 pyruvate or 1 3 pyruvate and 1 3 2-ketobutyrate to lead the formation of

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acetolactate or acetohydroxybutyrate, respectively. In the biosynthetic pathway, this is the basic step of the reaction for the generation of valine, leucine, and isoleucine in plants. Recently, many evidences indicated the diversion of catabolic products of amino acids to TCA cycle for energy generation to support growth, repair, and maintenance rather in the synthesis of storage proteins.

10.6 Chlorophyll and carotenoid biosynthesis Porphyrins are the main precursors for the synthesis of chlorophyll and heme. Porphyrins in plants are formed in plastid, mitochondrion, and cytoplasm and get complexed with protein and chelate with metals (either Fe or Mg) to function in metabolism. For some herbicides, porphyrins and their other derivatives are ought to be a good target looking at their inevitable requirement in crucial metabolic pathways (Rebeiz et al., 1994). All the enzymatic steps of porphyrin biosynthetic pathway are not good target for herbicides, except the enzyme protoporphyrinogen oxidase (PROTOX). For structurally diverse herbicides, this chloroplast membrane-bound enzyme is a very good target site (Dayan and Duke, 2003). Protoporphyrinogen oxidase (E.C. 1.3.3.4), the enzyme involved in the heme biosynthetic pathway, is the common enzyme in heme and chlorophyll biosynthesis. It catalyzes the oxidation of protoporphyrinogen IX to protoporphyrin IX. PROTOX inhibitors mode of action is unique because the inhibition of this enzymatic oxidation of protoporphyrinogen IX (Proto) led to the accumulation of the product outside the plastid (Dayan and Duke, 1997). Peroxidizing herbicides depend on light and are competitive inhibitors of PROTOX, causing desiccation and photobleaching. Among the known herbicides for inhibiting PROTOX, the dephenyl ethers, especially acifluorfen, is of great interest. The PROTOX -inhibiting herbicide acifluorfen cause accumulation of proto in darkness (Becerril et al., 1992). This accumulation of proto indicates toward the possible close link between PROTOX and the succeeding step in porphyrin synthesis (such as Mg chelatase in chlorophyll and Fe chelatase in heme). The synthesized protogen in the plastid stroma moves toward plastid envelope where PROTOX resides. Even without being converted to Proto by PROTOX, there is a movement of protogen to the cytoplasm (Lee et al., 1993, Lee and Duke, 1994). Fluorescence microscopic observation of accumulation of proto in the plasma-membrane of PROTOX inhibitor-treated plant cells was made (Lehnen et al., 1990). Photodynamic, proto accumulation especially at the plasma membrane (Lehnen et al., 1990), leads to quick and critical membrane damage upon sunlight exposure. Bleaching herbicides, such as picolinafen, flurtamone, flurochloridone, diflufenican, norflurazon and methoxyphenone, inhibit carotenoid biosynthesis. These herbicides cause inhibition of phytoene desaturation catalyzed by phytoene desaturase (PDS) in carotenoid synthesis. PDS and zetacarotene desaturase can be the targets of methoxyphenone. Commonly used herbicides of this class are mainly PDS inhibitors (Bo¨ger and Sandmann, 1998). Plastoquinone accepts e2 in carotenoid biosynthesis and in photosynthetic light reaction 2 e transport. Plastoquinone biosynthetic inhibitors are also herbicidal and cause phototoxicity (Bo¨ger and Sandmann, 1998). These inhibitors by inhibiting p-hydroxyphenylpyruvate

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dioxygenase (HPPD) interfere with homogentisate production from p-hydroxyphenylpyruvate. Isoxaflutole is a proherbicide and the degradation product, a diketonitrile is the inhibitor. The detoxypyrazolate, a metabolite of the herbicide pyrazolate, is also a potent HPPD inhibitor.

10.7 Conclusions Extensive uses of herbicides lead to its accumulation in ecosystem, thus inducing toxicity to crops and vegetation. Herbicides have multiple sites of action and can affect even a tolerant species as is evidenced by many researches where increased phytotoxicity affecting growth and development were reported. Herbicides interfere with light reaction of photosynthesis, with maximum damaging PSII and few PSI. Binding of herbicides to the QB site of the D1 protein facilitates the photodamage in PSII. There are also herbicides that block the e2 flow and affect the plastoquinone pool. Bipyridylium is a dual molecule and works by diverting e2 flow from PSI and converting itself into a reactive species that cannot be quenched by antioxidative system and thus cause an irreparable damage. Most potent herbicides are the peroxidizing and photobleaching herbicides that affect chlorophyll and carotenoid biosynthesis and also lead to oxidative stress. There is a close nexus, where hampered physiological processes create additional oxidative stress, and this over the one generated directly by herbicides exaggerate the damaging effect.

References Abdollahi, M., Ranjbar, A., Shadnia, S., Nikfar, S., Rezaie, A., 2004. Pesticides and oxidative stress: a review. Med. Sci. Monit. 10 (6), 141 147. Abedi, T., Pakniyat, H., 2010. Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). Czech J. Genet. Plant Breed. 46 (1), 27 34. Agostinetto, D., Perboni, L.T., Langaro, A.C., Gomes, J., Fraga, D.S., Franco, J.J., 2016. Changes in photosynthesis and oxidative stress in heat plants submitted to herbicide application. Planta Daninha 34 (1), 1 9. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373 399. Astiz, M., de Alaniz, M.J., Marra, C.A., 2009. Antioxidant defense system in rats simultaneously intoxicated with agrochemicals. Environ. Toxicol. Pharm. 28 (3), 465 473. Becerril, J.M., Duke, M.V., Nandihalli, U.B., Matsumoto, H., Duke, S.O., 1992. Light control of porphyrin accumulation in acifluorfen-methyl treated Lemna pausicostata. Physiol. Plant. 86, 6 16. Berger, S., Ferrell, J., Lion, R., 2012. Diagnosing Herbicide Injury in Cotton Series of the Agronomy Department, Uf/IFAS Extension. Bo¨ger, P., Sandmann, G., 1998. Carotenoid biosynthesis inhibitor herbicides: mode of action and resistance mechanisms. Pestic. Outlook 9, 29 35. Bonnemain, J.L., Chollet, J.F., 2002. L’arsenalphytosanitaire face aux ennemis des plantes. Conside´rations ge´ne´rales comptes rendus biologie 325, 1 6. Bouverat-Bernier, J.P., Gallotte, P., 1992. Chemical weed control post planting in Melissa officinalis. Herba Gallica 2, 23 37. Bowyer, J.R., 1991. In: Baker, N.R., Periwal, M.P. (Eds.), Herbicides-Topics in Photosynthesis. Elsevier, Amsterdam, p. 382. Brettel, K., 1997. Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim. Biophys. Acta 1318, 322 373.

Plant Life under Changing Environment

248

10. Responses of plants to herbicides: Recent advances and future prospectives

Chen, S., Yin, C., Strasser, R.J., Govindjee, Yang, C., Qiang, S., 2012. Reactive oxygen species from chloroplasts contribute to 3-acetyl-5-isopropyltetramic acid-induced leaf necrosis of Arabidopsis thaliana. Plant Physiol. Biochem. 52, 38 51. Chitnis, P.R., 1996. Photosystem I. Plant Physiol. 111, 661 669. Clay, D.V., Dixon, F.L., Willoughby, I., 2005. Natural products as herbicides for tree establishment. Forestry 78 (1), 1 9. Dalle-Donne, I., Aldini, G., Carini, M., Colombo, R., Rossi, R., Milzani, A., 2006. Protein carbonylation, cellular dysfunction, and disease progression. J. Cell Mol. Med. 10 (2), 389 406. Dayan, F.E., Cantrelh, C.L., Duke, S.O., 2009. Natural products in crop protection. Bioorg. Med. Chem. 17, 4022 4034. Dayan, F.E., Duke, S.O., 1997. Phytotoxicity of protoporphyrinogen oxidase inhibitors: phenomenology, mode of action and mechanisms of resistance. In: Roe, R.M., Burton, J.D., Kuhr, R.J. (Eds.), Herbicide Activity: Toxicology, Biochemistry and Molecular Biology. IOS, Washington, DC, pp. 11 35. Dayan, F.E., Duke, S.O., 2003. Herbicides: protoporphyrinogen oxidase inhibitors. In: Plimmer, J.R., Gammon, D. W., Ragsdale, N.N. (Eds.), Encyclopedia of Agrochemicals. J. Wiley, New York, pp. 850 863. Dayan, F.E., Watson, S.B., 2011. Plant cell membrane as a marker for light-dependent and light-independent herbicide mechanisms of action. Pestic. Biochem. Physiol. 101, 182 190. Dayan, F.E., Duke, S.O., Grossman, K., 2010. Herbicides as probes in plant biology. Weed Sci. 58 (3), 340 350. Etemadi-Aleagha, A., Akhgari, M., Abdollahi, M., 2002. A brief review on oxidative stress and cardiac diseases. Mid. East Pharm. 10, 8 9. Falk, J.S., Shoup, D.E., Al-Khatib, K., Peterson, D.E., 2006. Protox-resistant common waterhemp (Amaranthus rudis) response to herbicide applied at different growth stages. Weed Sci. 54, 793 799. Ferreira, L.C., Cataneo, A.C., Remaeh, L.M.R., Corniani, N., Fumis, T.F., de Souza, Y.A., et al., 2010. Nitric oxide reduces oxidative stress generated by lactofen in soybean plants. Pestic. Biochem. Physiol. 97, 47 54. Fo¨rster, B., Osmond, C.B., Pogson, B.J., 2005. Improved survival of very high light and oxidative stress is conferred by spontaneous gain-of-function mutations in Chlamydomonas. Biochim. Biophys. Acta 1709, 45 57. Gettys, L.A., Haller, W.T., 2009. Tolerance of selected bedding plants to four herbicides in irrigation water. Hortic. Technol. 19 (3), 546 552. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909 930. Grune, T., Davies, K.J., 2003. The proteasomal system and HNE-modified proteins. Mol. Aspects Med. 24 (4 5), 195 204. Hemaprabha, G., et al., 2013. Evaluation of drought tolerance potential of elite genotypes and progenies of sugarcane (Saccharum sp. hybrids). Sugar Technol. 15 (1), 9 16. Hess, F.D., 2000. Light-dependent herbicides: an overview. Weed Sci. 48, 160 170. Hock, B., Fedtke, C., Schmidt, R.R., 1995. Herbizide, Entwickling, Anwendung, wirkungen, nebenwirkunge. George Thieme Verlag, Stuttgart. Hoy, P.R., Stickey, J.S., 1881. Toxic action of black Walnut. Trans. Wisconsin State Hortic. Soc. 11, 166 167. Ivanov, S.V., Aleksieva, V.S., Karanov, E.N., 2005. Cumulative effect of low and high atrazine concentrations on Arabidopsis thaliana plants. Russ. J. Plant Physiol. 52, 213 219. ´ Jabłonska-Trypuc, A., 2017. Pesticides as inducers of oxidative stress. React. Oxygen Species 3 (8), 96 110. Janicka, U., et al., 2008. The effect of haloxyfop-ethoxyethyl on antioxidant enzyme activities and growth of wheat leaves (Triticum vulgare L.). Polish J. Environ. Stud. 17 (4), 485 490. Jung, S., 2003. Expression level of specific isozymes of maize catalase mutants influences other antioxidants on norflurazon induced oxidative stress. Pestic. Biochem. Physiol. 75, 9 17. Jung, H.I., et al., 2008. Resistance pattern and antioxidant enzyme profiles of protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice. Pestic. Biochem. Physiol. 91 (1), 53 65. Kumar, S., 2012. Effect of herbicides on carbohydrates, protein and electrophoretic protein bands content in Triticum aestivum L. Int. J. Food Agric. Vet. Sci. 2 (1), 13 25. Langaro, A.C., Agostinetto, D., Oliveira, C., Silva, J.D.G., Bruno, M.S., 2016. Biochemical and physiological changes in rice plants due to application of herbicides. Planta Daninha 34 (2), 277 289. Langaro, A.C., Agostinetto, D., Ruchel, Q., Garcia, J.R., Perboni, L.T., 2017. Oxidative stress caused by the use of preemergent herbicides in rice crops. Revista Cieˆncia Agronoˆmica 48 (2), 358 364.

Plant Life under Changing Environment

References

249

Lee, H.J., Duke, S.O., 1994. Protoporphyrinogen oxidizing activities involved in the mode of action of peroxidizings herbicides. J. Agric. Food Chem. 42, 2610 2618. Lee, H.J., Duke, M.V., Duke, S.O., 1993. Cellular localization of protoporphyrinogen-oxidizing activities of etiolated barley (Hordeum vulgare L.) leaves: relationship to mechanism of action of protoporphyrinogen oxidase inhibiting herbicides. Plant Physiol. 102, 881 889. Lehnen, L.P., Sherman, T.D., Becerril, J.M., Duke, S.O., 1990. Tissue and cellular localization of acifluorfeninduced porphyrins in cucumber cotyledons. Pest. Biochem. Physiol. 37, 239 248. Lukatkin, A.S., Gar’kova, A.N., Bochkarjova, A.S., Nushtaeva, O.V., da Silva, J.A.T., 2013. Treatment with the herbicide TOPIK induces oxidative stress in cereal leaves. Pest. Biochem. Physiol. 105, 44 49. Lydon, J., Duke, S.O., 1999. Inhibitors of glutamine synthesis. In: Singh, B.K. (Ed.), Plant Amino Acids. Marcel Dekker, New York, pp. 445 464. Malkomes, H.-P., 2006. Mikrobiologisch o¨kotoxikologische Bodenuntersuchungen von zwei zur Unkrautbeka¨mpfung mit hohen Dosierungen eingesetzten Fettsa¨ure-Herbiziden. UWSF Z Mitteilungen der Fachgruppe Umweltchemie ¨ kotoxikologie 18 (1), 13 20. und O Mansour, S.A., 2004. Pesticide exposure—Egyptian scene. Toxicology 198, 91 115. Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7 (9), 405 410. Molinari, H.B.C., et al., 2007. Evaluation of the stress-induce production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol. Plant. 130 (1), 218 229. Nohatto, M.A., Agostinetto, D., Langaro, A.C., de Oliveira, C., Ruchel, Q., 2016. Antioxidant activity of rice plants sprayed with herbicides. Trop. Goiaˆnia 46 (1), 28 34. Oliveira Junior, R.S., Constantin, J., Inoue, M.H., 2011. Biologia e manejo de plantas daninhas. Omnipax, Curitiba. Papadopoulous-Mourkidou, E., Karpouzas, D.G., Patsias, J., Kotopoulou, A., Milothridou, A., Kintzikoglou, K., et al., 2004. The potential of pesticides to contaminate the groundwater resources of the Axios river basin. Part II Monitoring study in the south of the basin. Sci. Total Environ. 321, 147 164. Pimental, D., 1995. Amount of pesticides reaching target pests: environmental impacts and ethics. J. Agric. Environ. Ethics 8 (11), 17 29. Quarles, W., 1999. Corn gluten meal: a least-toxic herbicide. Integr. Pest Manage. Pract. 21 (5/6), 7. Radwan, D.E.M., 2012. Salicylic acid induced alleviation of oxidative stress caused by clethodim in maize (Zea mays L.) leaves. Pestic. Biochem. Physiol. 102, 182 188. Rebeiz, C.A., Amindari, S., Reddy, N.K., Nandihalli, U.B., Moubarak, M.B., Velu, J.A., 1994. Delta-aminolevulinic acid-based herbicides. In: Duke, S.O., Rebeiz, C.A. (Eds.), Porphyrin Pesticides: Chemistry, Toxicology and Pharmaceutical Applications. ACS Symposium Series 559, pp. 48 64. Ruiz-Santaella, J.P., Heredia, A., Prado, R.D., 2006. Basis of selectivity of cyhalofop-butyl in Oryza sativa L. Planta 223 (2), 191 199. Scarfato, P., Avallone, E., Iannelli, P., De Feo, V., Acierno, D., 2007. Synthesis and characterization of polyurea microcapsules containing essential oils with antigerminative activity. J. Appl. Polym. Sci. 105, 3568 3577. Song, N.H., Yin, X.L., Chen, G.F., Yang, H., 2007a. Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere 68 (7), 1779 1787. Song, N.H., Yin, X.L., Chen, G.F., Yang, H., 2007b. Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere 69, 1779 1787. Trebst, A., 2007. Inhibitors in the functional dissection of the photosynthetic electron transport system. Photosynth. Res. 92, 217 224. Tripathy, B.C., Mohapatra, A., Gupta, I., 2007. Impairment of the photosynthetic apparatus by oxidase stress induced by photosensitization reaction of protoporphyrin IX. Biochim. Biophys. Acta 1767 (6), 860 868. Varshney, S., Hayat, S., Alyemeni, M.N., Ahmad, A., 2012. Effects of herbicide applications in wheat fields is phytohormones application a remedy? Plant Signal. Behav. 7 (5), 570 575. Weichenthal, S., Moase, C., Chan, P., 2010. A review of pesticide exposure and cancer incidence in the agricultural health study cohort. Environ. Health Perspect. 118 (8), 1117 1125. Yoon, J.Y., Shin, J.S., Shin, D.Y., Hyun, K.H., Burgos, N.R., Lee, S., et al., 2011. Tolerance to paraquat-mediated oxidative and environmental stresses in squash (Cucurbita spp.) leaves of various ages. Pestic. Biochem. Physiol. 99, 65 76.

Plant Life under Changing Environment

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10. Responses of plants to herbicides: Recent advances and future prospectives

Young, S.L., 2004. Natural Product Herbicide for Control of Annual Vegetation Along Roadside, 4. West Central Research and Extension Centre, North Platte. Zhang, J.J., Lu, Y.C., Zhang, J.J., Tan, L.R., Yang, H., 2014. Accumulation and toxicological response of atrazine in rice crop. Ecotoxicol. Environ. Saf. 102 (1), 105 112. Zhou, Q., Liu, W., Zhang, Y., Liu, K.K., 2007. Action mechanisms of acetolactate-synthase-inhibiting herbicides. Pestic. Biochem. Physiol. 89, 89 96.

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11 Effects of abiotic stresses on sugarcane plants with emphasis in those produced by wounds and prolonged post harvest periods Elena Sa´nchez-Elordi1, Eva M. Dı´az1, Roberto de Armas2, Rocı´o Santiago1, Borja Alarco´n1, Carlos Vicente1 and Marı´a Estrella Legaz1 1

Team of Intercellular Communication in Plant Symbiosis, Department of Genetics, Physiology and Microbiology, Faculty of Biology, Complutense University, Madrid, Spain 2Department of Plant Biology, Faculty of Sciences, Havana University, Havana, Cuba

11.1 Introduction Sugarcane (Saccharum officinarum L.) is the most widespread crop grown for sugar production. Therefore knowledge of the environmental circumstances that determine their stress is important to improve the production of sucrose and ethanol, two products of primary interest in the food and fuel industries. The genus Saccharum comprises six species of different degree of polyploidy, two of which are wild (Saccharum robustum and Saccharum spontaneum) and four are hybrids obtained by genetic improvement techniques (Saccharum sinense, Saccharum barberi, Saccharum edule, S. officinarum). Specifically, S. officinarum has as its ancestors, S. spontaneum, Miscanthus sinensis, and Erianthus arundinaceus (Daniels and Roach, 1987). The currently cultivated commercial varieties are complex hybrids of two or more species (Julien et al., 1988). This is the case of S. officinarum and S. spontaneum, for which the hybrid formed maintains the efficient level of productivity of the first species and the high resistance to diseases of the second (Cox et al., 2000).

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Sucrose in S. officinarum is synthesized and accumulated in the parenchymatous cells of the stems, although some soluble polysaccharides may be transiently produced (Covacevich and Richards, 1977; Roberts et al., 1985). This is accomplished by a decrease in the yield of sucrose production and a product whose appearance and properties produce rejection from the consumer is obtained. Several glycoproteins collaborate in the loss of sugar recovery. The colligative properties of the peptide moiety of these glycoproteins favor their attachment to the underside of the sucrose crystals, which makes it difficult to aggregate these crystals in star-shaped sets (Fontaniella et al., 2003). The glycidic moiety of the sugarcane glycoproteins, by themselves, or the polysaccharides produced by other sugar plant species do not prevent the formation of such crystalline complexes (Vicente et al., 2000). This can be interpreted as a probe that the binding of sugarcane glycoproteins to sucrose crystals is due to the formation of hydrogen bonds between some amino acids of the peptide moiety and sucrose. In addition, sugar production is influenced by several unfavorable abiotic factors, such as temperature, salt stress, nutritional deficits, drought or incorrect preprocessed storage systems, which reduce its yield in the production and accumulation of the abovementioned metabolite.

11.2 Heat and cold stress Heat stress is defined as the temperature that slows or stops the growth of a plant, irreversibly damaging it. Excessive heating causes excessive transpiration, leading to dehydration. Sugarcane leaves try to minimize this effect by foliar rolling, which is achieved by the expansion of the volume of their bulliform cells (Fig. 11.1). By subjecting two sugarcane cultivars, CP-4333 and HSF-240, to thermal stress conditions for 72 hours, it was found that CP-4333 cv rolled their leaves faster than HSF-240. A decrease in fresh weight was found for a constant dry weight and leaf area, which means that both fresh to dry weight ratio and leaf water potential decrease. The results suggest that improved heat tolerance in sugarcane CP-4333 cv was accompanied by reduced water loss per leaf, increased leaf winding speed, and faster reversal of these effects during recovery. When plants of Co 86032 cv. of sugarcane were maintained for 25 hours at 40 C, the amount of soluble sugars, free proline, and glycine was observed to increase linearly. However, none of these metabolites have osmotic significance and, therefore, cannot be considered as defensive substances against desiccation caused by high temperature. An increase in the total phenol content induced by thermal stress may be related to the prevention of oxidative damage. Heat stress increases the production of transcripts for peroxidase and superoxide dismutase as well as their enzymatic activities, required to protect the plant cells against oxidative damage. The analysis of 13 different genotypes of sugarcane subjected to thermal heat stress shows that, in all cases, lipid peroxidation and membrane instability increase, although the genotypes S-2003-US-778, S-2003-US-694, CPF-237, and Co-1148 show to be heat tolerant by reduced formation of malondialdehyde (MDA) during thermal stress. On the other hand, thermotolerance is usually associated with the accumulation of trehalose. A mutation that suppresses the gene for trehalose-6-phosphate (T6P) synthase (TPS) transforms the resistant plant into heat sensitive. Trehalose is an

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FIGURE 11.1

(A) SEM micrograph of the cross section of a sugarcane leaf in sagittal vision, showing the surface of the epidermis and the bulliform cells. (B) SEM micrograph of the magnification of a cross section of sugarcane leaf showing the bulliform cells. SEM, scanning electron microscopy.

osmotic of high solubility in water that stabilizes cytoplasmic proteins, avoiding their thermal denaturation. Cold is a major abiotic stress that limits the production of tropical and subtropical crops in new production areas. Sugarcane (Saccharum spp.) comes from the tropics but is grown mainly in the subtropicals, where it often encounters cold stress. Sugarcane is highly sensitive to freezing, either under natural or experimentally induced conditions. The tissues of the stems suffer a notable deterioration, with the appearance of cracks in the cuticle, which affect more internal tissues. Eggleston et al. (2004) demonstrated remarkable changes in the main indicators of freeze deterioration, such as increased juice viscosity or decreased pol-filterability. In areas damaged by frostbite, Leuconostoc mesenteroides frequently develops, contributing to the deterioration by synthesizing their own dextran, levanes, and alternans, as well as mannitol. This polyalcohol is produced by a bacterial mannitol dehydrogenase, and it is considered by the authors to

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be the best indicator of changes in viscosity and pol-filterability of the juices. Logically, the production of mannitol by Leuconostoc is related to the use of sugarcane sucrose by the bacteria, also related to the decrease of the plant’s own dextran and the decrease in the viscosity of the juices. In general, sugarcane plants, growing at 4 C for 38 days, decrease their chlorophyll content as the days with low temperature increase, as well as the values of net photosynthesis and stomatal conductivity. Cold stress also decreases the maximum efficiency value of light energy conversion, the current quantum efficiency of photosystem II, the reaction center’s excitation energy capture, and electron transfer rate (Tang et al., 2015). MicroRNAs (miRNAs) have proven to be an important gene-regulation mechanism that is active in sugarcane and many other plant species under abiotic stress conditions. This is logical since the perception of signals arising from extreme environmental conditions would be directly related to the outbreak of epigenetic mechanisms of adaptation. From 412 miRNAs identified in sugarcane plants by Yang et al. (2017), 62 showed a significant differential expression under cold stress. This could be related to lower levels of reactive oxygen species (ROS) and higher anthocyanin content. In addition, as demonstrated by Thiebaut et al. (2012), the production of miRNAs was provoked by subjecting sugarcane plants to a prolonged cold period. The analysis of these transcripts by RT-PCR showed that the production of one of them, in particular miR319, was upregulated after 24 hours of exposure of the sugarcane to low temperatures (4 C) and that its expression was carried out both at the roots and at the buds of the seedlings. The production of this microRNA could also be triggered by a treatment with abscisic acid. The targets of miR319 were some transcription factors, such as TCP-PCF5, TCP-PCF6, GAMyb, a protein kinase, and a fasciclin-like glycoprotein, a subclass of arabinogalactan proteins that have putative domains for cellular adhesion, known as fasciclin domains. On the other hand, Park et al. (2015), working with S. spontaneum, demonstrated that a homolog of a major intrinsic protein gene type NOD26 (SspNIP2), which encodes for a boric acid transporter, was expressed B2.5 times more than in the control not cold-treated at 30 minutes after the start of treatment at 4 C, and remained induced during 24 hours of cold treatment. Nogueira et al. (2003) identified 20 expressed sequence tags consisting of novel coldresponsive genes which codified for cellulose synthase, ABI3-interacting protein 2 (ABSCISIC ACID INSENSITIVE3, a transcription factor of the abscisic acid signal transduction pathway), a negative transcription regulator, and a phosphate transporter. This ABI3-interacting protein 2 as well as other different ones are involved in the beginning of the plant’s cold acclimation by intervening in the increase of the cytoplasmic Ca21 concentration of regulating the influx of Ca21 through the membrane and its exit from the vacuole through the tonoplast.

11.3 Nutrition-related stresses Sugarcane is a plant species with a great ability to produce biomass, which implies a high requirement of K1. Therefore, soil deficient in this cation or inadequately fertilized with products of low K1 content diminishes plant growth. For example, Zeng et al. (2015) have performed a transcriptome profiling of sugarcane plants subjected to stress deficit in

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potassium and have found a noticeable increase in the activity of peroxidase enzyme, clearly related to stress processes. Pyruvate dehydrogenase 2, which would keep the respiratory process unchanged, was also increased as well as a phosphoglycerate kinase was probably involved, together with the decrease in phosphofructokinase and glycerate 3-P dehydrogenase, in gluconeogenesis and a glutathion S-transferase, related to the metabolism of ROS. The search for homologous genes related to the production of antioxidants for sugarcane in the SUCEST (Soares Netto, 2001) database resulted in the description of homologs for cytosolic monodehydroascorbate reductase and GSH-dependent dehydroascorbate reductase, as well as γ-glutamylcysteine synthetase, the first step in glutathione biosynthesis. However, this requirement for a continuous supply of K throughout the life of the plant presents a drawback, according to Watanabe et al. (2016), since an excess of this cation may decrease the concentration of sucrose accumulated in the stem. The most abundant ions in cane juice, analyzed for 3 consecutive years, were potassium and chlorides. The amount of both ions could be inversely related to the concentration of sucrose occurring in the juices. As the electrical conductivity of the juices increased (as a consequence of the increase of K and Cl), the sucrose concentration decreased. This means that an excessive fertilization with KCl can give high yield in biomass production but low yield in industrial sugar efficiency. Alexander (1967) already demonstrated that in sugarcane plants grown in sand, deficiencies of nitrogen, phosphorus, potassium, and calcium were gradually produced. All plants subject to this limited nutrition regime accumulated more sucrose in the leaves than the control plants, regardless of the reduced nutrient content. In each case, the increase in sucrose concentration was obtained before a net nutrient deficiency level was reached. This seems to indicate an imbalance of nutritional elements rather than the deficiency itself as the cause of an unequal distribution of sucrose. All plants subjected to limited nutrition revealed a decrease in amylase activity as the sucrose concentration increased. Peroxidase was greatly stimulated under all treatments, while phosphatase decreased with reduced nitrate and phosphorus supplement but, in general, did not vary significantly with potassium and calcium deficits. Alterations in the mineral nutrition of plants cause chlorosis through different molecular mechanisms. The growth of sugarcane plants on iron-deficient soils causes chlorosis due to a decrease in the formation of hemo-groups, while an excess of manganese in acid soils causes similar chlorosis and ratooning, and morphology of multiple short shoots. In this case, the chlorophyll deficiency appears to be due to a substitution of Mg21 by the excess foliar Mn21. In addition, Mn21 can act as a catalyst in the production of ROS, which would decrease the amount of chlorophyll, a parameter that would also be negatively affected by Mn21 inhibition of those chlorophyll biosynthetic reactions that specifically require Fe21, according to Huang et al. (2016).

11.4 Salt stress Among the mineral cations of the soil, sodium is clearly an unfavorable element for the growth of sugarcane, so much so that cane is cultured in the vicinity of the ocean or on

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soils of marine origin in many tropical countries. The most evident effects of salinization on sugarcane affect growth in general, although root growth is more adversely affected than that of the bud. The chlorophyll content showed a tendency to decrease (chlorosis), and the dry matter yield of plants decreased, although tolerant somaclonal varieties do so at a slower rate than those of sensitive varieties. The content of Cl2 and Na1 in buds and roots increases (Shomeili et al., 2011). Salinity can induce water deficit and oxidative stress, which causes alterations of biomolecules and cell damages. However, plants can implement defense, metabolic, or structural mechanisms that can prevent or at least minimize damage. To analyze tolerance of sugarcane plants to salt stress, two genotypes of sugarcane (RB931011 and RB872552), cultured in Brazil, grew up in vitro under saline stress for 20 days in the presence or absence of 100 mM NaCl. Both genotypes suffered a visible reduction in membrane integrity, a decrease in total soluble proteins, and the maintenance or increase of endogenous proline content. A supply of 20 mM of exogenous proline decreased the accumulation of Na1 in proportion to the time of treatment with the amino acid. In both genotypes, the activity of some antioxidant enzymes, such as catalase, ascorbate peroxidase, and peroxidase, increased with NaCl salinization, this effect being more pronounced in genotype RB931011 (Medeiros et al., 2015). Similar results were obtained for sugarcane CoC 671 and Co 86032 cvs., used in India, grown on increasing the concentration of NaCl (from 50 to 250 mM). In these conditions, several parameters, such as the relative growth rate (RGR), membrane damage rate (MDR), MDA accumulation, soluble proteins, osmolites (proline, betaine, and glycine), ions (Na1 and K1) and antioxidant enzymes, such as peroxidase, ascorbate peroxidase, guaiacol peroxidase, catalase, and superoxide dismutase, were measured. RGR decreased, and MDR and MDA levels as well as free proline after salinization increased. CoC 671 cv. was more tolerant to Na1 (150 mM) than Co 86032 cv. (Karpe et al., 2012). In relation to the accumulation of osmotics, the fact that small accumulations of trehalose have been found in sugarcane plants under saline stress connects with that experienced in other grasses. For example, the addition of low concentrations of exogenous trehalose to rice plants maintains the root integrity, avoiding an aberrant cell division and protects root cells from strong saline stress (Garcia et al., 1997). This protection could be explained by the conservative effect of trehalose on ion pumps, which selectively keep excessive quantities of sodium from chloroplasts. However, trehalose did not prevent salt accumulation in plant cells. Although the soluble protein content in plants subject to saline stress decreases in general, a particular protein can increase its amount as soluble protein. For example, sugarcane leaf cells contain a high proportion of cell wall particulate RNase, while its occurrence as cytoplasm-soluble protein is usually low. However, when the plants are subjected to progressive saline stress, a part of the particulate RNase turns to cytoplasm, whose water content can be preserved for a certain period of time, whereas the cell wall becomes dehydrated as a result of the increase in osmotic pressure (Fig. 11.2). In addition to these enzymes related to oxidative stress, other proteins are expressed differently in control plants and plants under saline stress. Proteins involved in sugar catabolism, such as fructose 1, 6-bisphosphate aldolase, a germin-like protein, and glyceraldehyde-3-phosphate dehydrogenase were over-expressed under saline stress conditions, while the thermal shock protein 70 was expressed only in salinized plants

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11.5 Drought

FIGURE 11.2 Occurrence of pelletable RNase in the cell wall of sugarcane leaves (circles) of cytoplasmic, soluble RNase (triangles) as a function of the concentration of external NaCl in irrigation water.

(Merlot et al., 2001). Other proteins, such as a calcium-dependent protein kinase, protein complexes of photosystem I, as well as a phospholipase D, were more abundant in the tolerant RB855536 cv. under salt stress (Passamani et al., 2017). Alexander (1968) assigned to silicon a decisive role in sugarcane metabolism by claiming that it could be an invertase inhibitor, a supposed role that was rejected by Cheong et al. (1971). In addition, Camargo et al. (2017) found that the fertilization with silicon of two cvs., one sensitive and one resistant to drought, significantly increased not only the growth of the plant but also the yield in the recovery of sugar from the juices extracted from the stems.

11.5 Drought Lack of water is a major abiotic stress that retards plant growth and decreases crop productivity. Shallow root system of sugarcane makes the plant susceptible to drought without serious damage when the ripening is ending. This is understood as the phase of maximum sucrose accumulation. In addition to stunted growth, drought can cause a decrease in photosynthetic efficiency and a severe loss in the amount of sucrose that can accumulate during the earlier stages of development. Key enzymatic activities, such as RuBisCO, nicotinamide adenine dinucleotide phosphate (NADP)-malate dehydrogenase, NADP-malic enzyme, and pyruvate Pi dikinase, decreased in drying sugarcane leaves, while this stress did not affect the activity of PEP carboxylase (Vu and Allen, 2009). Other physiological effects caused by drought in sugarcane plants are usually related to the efficiency of the canopy in capturing light, leaf temperature, stomatal conductivity, and therefore transpiration, physiological parameters that are always reduced in the water-deficit conditions. However, resistant cultivars can counteract some of these effects, such as efficiency in capturing light, by boosting the activity of genes that encode for chloroplastic, antenna-forming proteins associated with a/b chlorophyll (Ngamhui et al., 2012). Other chloroplastic proteins related to antioxidant activities, such as copper zinc superoxide dismutase (SOD), peroxiredoxin of two cysteines (2-Cys Prx), superoxide dismutase

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[manganese] (SOD[Mn]), and isoflavone reductase, were also upregulated as a consequence of drought. One of the upregulated genes as a response to induced water stress, Scdr1 (sugarcane dry-responsive 1) was described by Begcy et al. (2012). This gene encodes for a protein enriched with high content of proline and cysteine. Scdr1 is phylogenetically related to its homologous gene in Sorghum, Zea, Brachypodium, and Oriza. Although the expression of Scdr1 in different varieties of sugarcane plants has not shown a clear association with drought tolerance, its overexpression in transgenic tobacco plants increases photosynthetic efficiency, water content, amount of biomass accumulated, seed-germination rate, chlorophyll content and decreases the accumulation of ROS. But not only does polymerized proline appear in specific proteins as a response to drought. Using two sugarcane cultivars, one tolerant (RB867515) and the other sensitive (SP86-155) to drought, Vantini et al. (2016) showed that the level of free proline in roots of the resistant cultivar increased by 25% compared to what happened in sensitive cv. Plants subjected to experimental drought were able to maintain the turgor for five days when stress was moderate and withstand the effects of severe water stress for 10 days. The authors hypothesize on the action of proline by triggering a cell-signaling system that maintains turgor of the cells. The maintenance of cell morphology, derived from the preservation of turgor pressure, may be influenced by the activation of drought-induced genes encoding for actin and tubulin, constituents of the cytoskeleton (de Andrade et al., 2017). Other genes, whose expression is increased by drought in resistant cvs., are related to the production and accumulation of sucrose and to the maintenance of the water potential. In this sense, Iskandar et al. (2011) have logically found upregulated genes related to proline metabolism, such as ornithine aminotransferase and proline oxidase, dehydrin, the protein LEA (late embryogenic abundant), which is a protein that protects other proteins from aggregation induced by desiccation and all of these are related to the resistance to the drought, and trehalase (trehalose accumulation is normally identified as a symptom of water deficit), spermidine synthase, and asparagine synthase.

11.6 Stress produced by mechanical injuries Carbon metabolism in sugarcane produces not only sucrose but also several soluble polysaccharides. This set includes arabinogalactans (Roberts et al., 1985), starch-like glucose polymers (Covacevich and Richards, 1977), and heteropolymers composed by fructose and galactitol in variable proportion (Legaz et al., 1990). Mechanical injuries, cutting techniques, and inadequate storage activate the appearance of these polysaccharides in sugarcane juices. Difficulties in transporting the cut stems to the factories sometimes mean that these stems remain abandoned on the ground for hours or even days, thus initiating deterioration in the cutting areas. Glucans, colloidal fructans and soluble high molecular mass polysaccharides (HMMC) and mid molecular mass polysaccharides (MMMC), such as sarkaran (Bruijn, 1970), have been found after stem deterioration due to the detriment of accumulated sucrose. The greater the amount of heteropolysaccharides in juices, the greater the number of wounds inflicted on the stems

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259 FIGURE 11.3 (A) Changes in the amount of soluble, total polysaccharides as a function of a number of mechanical injuries in stalks of Jaronu´ 60-5 sugarcane cultivar. (B) Changes in the amount of total soluble polysaccharides in juices obtained from stalks of the cv. Cuba 374-72 during post collection impairment. Source: Modified from Fig. 11.4, from Legaz, M.E., de Armas, R., Millanes, A.M., Rodriguez, C.W., Vicente, C., 2005. Heterofructans and heterofructan-containing glycoproteins from sugarcane: Structure and function. Recent Res. Devel. Biochem., 6, 31 51.

(Fig. 11.3A), the age of the plants, the oxygen content, and the time between cutting the stem and grinding (Fig. 11.3B) (Rodriguez et al., 1985; Valdes and Rodriguez, 1982a). Occasionally, the production of these soluble polysaccharides has been interpreted as an attempt to heal the wound (Valdes and Rodriguez, 1982b). However, the secretion of such macromolecules in the wound area has been shown not to cause an occlusion of the injury produced, although an increase in the lignin production and in the mechanical resistance of sclereids has been observed. Varietal differences of this type of polysaccharides have also been reported. These HMMC and MMMC can be separated by ion-exchange chromatography into two different fractions, one being preferably of anionic nature, consisting of different glycoproteins, and the other, entirely cationic, being exclusively of protein nature (Fig. 11.4). Therefore, the so-called hitherto HMMC and MMMC should be considered high molecular

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FIGURE 11.4 Diagram of anionexchange chromatography on a DEAESephadex A60 column of the content in carbohydrates and proteins of sugarcane juice, Jaronu´ 60-5 cv., eluted in an increasing concentration gradient of NaCl in the mobile phase. Source: Modified from Fig. 11.1, from Legaz, M.E., Pedrosa, M.M., de Armas, R., Rodrı´guez, C.W., de los Rı´os, V., Vicente, C., 1998. Separation of soluble glycoproteins from sugarcane juice by capillary electrophoresis. Anal. Chim. Acta, 372, 201 208.

mass glycoproteins (HMMG) and mid molecular mass glycoproteins (MMMG). These polysaccharides, free or as a glycidic component of glycoproteins, are composed by β-1,2 homofructane domains to which units, or groups of units, of galactitol are added via ether links (Legaz et al., 1995). HPLC analysis of sugarcane glycoproteins confirmed that it neither contained free sucrose nor monosaccharides. The proteomic analysis of this fraction reveals that it is composed of at least six different glycoproteins: arginase, chitinase, β-1,3 and β-1,4-glucanase, and two dirigent proteins. The total hydrolysis of the glycidic moieties of sugarcane glycoproteins results in free fructose and galactitol. The quantitation of the acid hydrolysis of the products of their glycidic moieties reveals differences in the degree of polymerization for the different glycoproteins. Those with a medium molecular mass, from 15 to 70 kDa, contain a polymer [Fructose2: Galactitol3]n, while those with a higher molecular mass, bind a polysaccharide type [Fructose4: Galactitol5]n. Since invertase is able to hydrolyze β(1-2) linkages, it can be deduced that the glycidic moiety of the sugarcane glycoproteins consists of domains β(1-2) fructofuranoside, which can be hydrolyzed by invertase, between which fructose-galactitol heteropolymeric segments are mixed or added. The ether bond between fructose and galactitol can only be broken by acid hydrolysis, not by invertase action. Obviously, the half β-1,2-fructan of the glycidic moiety of sugarcane glycoproteins will be synthesized, like the rest of the fructans, by the consecutive action of sucrose:sucrose fructosyltransferase, which produces the corresponding trisaccharide, followed by a fructan:fructan fructosyltransferase which lengthens the chain. This means that the alternative synthesis of heterofructans after an injury will result in an extra consumption of sucrose that will not be stored. These heterofructans are subsequently found as glycidic moieties of glycoproteins, but its release after a mechanical injury of the stem will be unknown. When these glycoproteins were produced by post collection impairment, accumulation of glycoproteins was a transient process, since their amount increased at the second day of impairment to decrease and stabilize later. This clearly indicated that sugarcane stalks produced enzymes to catabolize soluble heterofructans when required.

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To study the occurrence of enzymes for heterofructan catabolism in sugarcane, protein in juices was reversibly precipitated with 80% (v/v) acetone. The precipitate was recovered by centrifugation, dried in air, and redissolved in the adequate buffer. The protein was assayed by using as substrates the glycidic moiety of sugarcane glycoproteins and a suspension of purified cell walls obtained from parenchymatous cells of sugarcane stalks. Acetone-precipitated protein from sugarcane juice obtained from stalks of cv. C734-72 was assayed against heterofructans, at pH 7.5, for 1 hour at 30 C, without cofactor addition. The appearance of reducing sugars in the reaction mixture and the appearance of polymers with a molecular mass lower than that of the unmodified substrate clearly indicated that parenchymatous cells contained enzymes for heterofructan degradation. Valuable amounts of HMMG and MMMG can be obtained from purified parenchymatous cell walls by the action of these juice glycosidases (Martı´nez et al., 1990a,b), revealing that soluble heterofructans could be “dissolved” by enzyme action into cytoplasm from cell wall insoluble, structural precursors. Glycosidase activity was revealed as dependent on Mn21 that could be partially substituted by Mg21. This glycosidase works optimally at pH 6.0, while at pH 7.5, it is inactive against HMMG and weakly active against MMMG. The optimum temperature for the glycosidase-catalyzed reaction is 30 C, being completely inactivated at 70 C. Its pI was shown to be 6.5 although an isoform of pI 8.5 copurifies with the main enzyme. This is a molecular mass monomer of 13.2 kDa (Legaz et al., 1990). Some varietal differences for glycosidase activity have been observed. The activity of the purified enzyme from cv 9-month-old C374-72 plants against high molecular mass glycoproteins was higher than that found against mid-molecular mass glycoproteins, whereas the inverse behavior was observed for the protein purified from cv. Ja 60-5. Cellfree extracts obtained from the cv. B63118 with the same age did not contain detectable hydrolase activity. The study of a preparation of C374-72 glycosidase, purified at homogeneity, shows that the optimal hydrolase activity was achieved for a Mn21 concentration of 2.5 mM in the reaction mixtures. Concentrations of the cofactor were higher than that determined as the optimal produce inhibition of the enzyme. The kinetics of manganese binding to glycosidase has been studied by equilibrium of dialysis. Incubation of purified enzyme with the cofactor was carried out at 30 C with continuous stirring for increasing times. Equilibrium in dialysis, which implies the maximum value of binding of Mn21 to glycosidase, was obtained after 12 hour dialysis. By maintaining this unchanged time value, bound Mn21 exponentially increases as a function of the concentration of total Mn21 from 0.1 to 0.55 μM. From this value, the amount of bound Mn21 rapidly decreased to stabilize from 0.73 μM (Legaz et al., 1991). Mn21 binds to the glycosidase molecule according to a positive cooperativity model, as deduced from the corresponding Scatchard plot, which included two different points for binding the effector to the protein, as deduced from the corresponding Hill plots. Mn21 concentrations, higher than 0.55 μM, reverse this binding kinetics. This reveals that glycosidase behaves as a hysteretic enzyme when it interacts with its effector. The time-course of glycoprotein variations during post collection impairment experiments can strictly be correlated to the development of glycosidase activity and to the content of free Mn21 of extracted juices from impaired stalks.

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Under an industrial point of view, these glycoproteins in sugarcane juices change the pattern of the crystallization of sucrose, as mentioned above. In general, these glycoproteins delay the appearance of the first nuclei, hinder the association of individual crystals to form agglomerates or star-like nuclei, and increase the degree of surface erosion of the formed crystals. Using glycoproteins labeled with fluorescein isothiocyanate, Sa´nchezElordi et al. (2017) observed that the adhesion of these glycoproteins to the sucrose crystals is carried out mainly on the edges thereof, never on their flat faces, and never penetrating inside them, although they may move along its outer surface. The fluorescence diffuses in the zones of rupture or abrasion, indicating that the appearance of such accidents releases the proteins adhered to the free solution. These glycoproteins have also been considered defense mechanisms against phytopathogenic bacteria and fungi (Legaz et al., 2011; Sa´nchez-Elordi et al., 2016). Therefore, the role of these glycoproteins, poured into the injured tissue area, could exclusively have the function of protection systems against possible infections by fungi or phytopathogenic bacteria that try to take advantage of this wound as an infective entry route into the plant. As can be seen in Fig. 11.5, the wounds inflicted in the sugarcane stalks with a scalpel remain FIGURE 11.5 (A) Mechanical injuries produced with a scalpel in sugarcane stalks, cv. Louisiana 55-5, in (B) transversal or (C) longitudinal orientation. (D) Superficial aspects of both injuries 8 days after the mechanical injury.

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open for 8 days after the mechanical injury, the edges are separated, dried and clean, without any excrescence or deposits of occlusion material. The only visible difference with the unwounded stem is the increase in reddish color of the epidermis by an accelerated induction of flavonoid biosynthesis, mainly naringenin, luteolin, luteolin-7-glucoside, and apigenin (Legaz et al., 1998). These flavonoids collaborate in wound asepsis and, above all, act as antioxidants against the ROS that the plant tissue accumulates after mechanical injury. Cross sections of the injured zones have been analyzed by light and fluorescence microscopy, using an excitation light of 462 nm to observe the autofluorescence of lignins. In Fig. 11.6A the epidermal tissue can be observed, near which accumulations of docking cells and vascular bundles, containing xylem and phloem and surrounded by peripheral fibers are arranged. These sclereids, as well as docking cells, show green autofluorescence of lignins, excited by blue light (Fig. 11.6B). In the wound area, the packets of docking cells

FIGURE 11.6 Micrographs obtained by light (A, C, and E) and fluorescence (B, D, and F) microscopy of cross sections of sugarcane stalks, Louisiana 55-5 cv., control without having suffered mechanical injury (A and B), or stems stabbed with a scalpel (C F), as shown in Fig. 11.5A. ep, epidermis; flv, flavonoids; p, parenchima; ph, phloem; sc, sclereids; vb, vascular bundle.

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can be observed separated from the epidermal tissue by mechanical injury, with their cell walls strongly thickened (Fig. 11.6C) due to new deposits of lignin (Fig. 11.6D). In some areas of the intact epidermal tissue, discrete and reddish accumulations can be observed under a light microscope, corresponding to neosynthesized flavonoids in response to mechanical injury (Fig. 11.6E). In addition, an increase in the autofluorescence of lignins from vascular beam fibers (Fig. 11.6F) can be seen. It therefore appears that the desiccation and cleaning of the open edges of the wounds, shown in Fig. 11.5C and D, would be due to an increase in the lignification of the tissues surrounding the mechanical injury, both on the surface and in depth. This would be related to the ability of glycoproteins, synthesized and secreted after a wound, to modulate dirigent proteins to increase lignin synthesis or, on the contrary, to synthesize lignans as defense molecules (Legaz et al., 2018). Wounds often cause an accumulation of ROS in plants. Minibayeva et al. (2009) have identified several of the proteins involved in both ROS production and detoxification. An exocellular peroxidase would be responsible for the production of the superoxide anion (Od22 ), whereas superoxide dismutase acts as a potent antioxidant.

11.7 Sucrose synthesis and partitioning during abiotic stress Approximately 70% of the sugar used in food comes from sugarcane and, in some cases, this plant is also used in the production of ethanol and electricity. Sucrose is synthesized in the leaves as a transformation pathway for the primary products of photosynthesis, trioses-P and hexoses-P, into a translocable disaccharide. Sucrose is formed in the cytosol of photosynthetic cells from uridine diphosphate (UDP)-glucose and fructose-6-P, formed in the Calvin cycle thanks to a fructose-bisphosphatase, by the action of a sucrose6-P synthase (SPS), which forms sucrose-P with UDP liberation. A new enzyme, sucrose-P phosphatase (SPP), dephosphorylates sucrose-P to sucrose with release of Pi. The production of sucrose can be negatively regulated by the action of a phosphofructokinase 2, which would transform part of the pool of fructose-6-P into fructose-2,6-bisphosphate, a potent inhibitor of fructose-bisphosphatase (Fig. 11.7). The sucrose synthesized in the leaves is transported to the stem, via phloem, and its accumulation in the parenchymatous cells is carried out by means of a post-phloem transfer system which can follow two different ways: a symplastic way, through plasmodesmata, the preferential route in the internodes of the cane, or an apoplastic way, through the open spaces of the cell wall. This apoplastic transfer involves hydrolysis of the disaccharide by a particulate invertase of the cell wall. Both hexoses resulting from such hydrolysis and the remaining nonhydrolyzed sucrose may enter the parenchymatous cell through specific transporters. Several of these transporters have been described for sugarcane. Genes encoding these carriers, such as ShSUT1, ShSUT2, and ShSUT4, were abundantly expressed both in leaves and stems and, in particular, ShSUT1 in leaves was highly expressed in vascular bundles (Wang et al., 2017). Sucrose entering the cell by the symplastic route can also be hydrolyzed by cytoplasmic neutral invertase or vacuolar neutral invertase. Sucrose is stored both in vacuoles and cell wall spaces (Wang et al., 2013). An alternative to the use of hexose 6-P and UDP pools in plants is the production of trehalose, a disaccharide that has long been thought to be present in plants due to bacterial

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FIGURE 11.7 The alternative use of UDP-glucose pool in the biosynthesis of sucrose or trehalose.

contamination, until genes were identified in Arabidopsis with very high homology with bacterial TPS and TPP. These genes encode for TPS and T6P phosphatase (TPP), respectively, the two enzymes responsible for the disaccharide synthesis. Transglycosylation catalyzed by TPS is practically irreversible under physiological conditions. Both enzymes, synthase and phosphatase, are usually aggregated in a complex called trehalose synthase. The final result is a trimeric protein under the control of three different genes: TPS1, which encodes for a 56 kDa synthase; TPS2, which encodes for the phosphatase subunit of 102 kDa; and TPS3, which encodes for a regulatory protein. It has sometimes been argued that the low concentration of trehalose in sugarcane and other plant species is due to high trehalase activity. To improve the production of trehalose in sugarcane hybrids, two transgenes were introduced into the sugarcane genome (O’Neill et al., 2012): TPS/phosphatase (TPSP), to increase the biosynthesis of trehalose, and a transgene RNAi specific for trehalase, to nullify the catabolism of trehalose. In the lines that expressed this RNAi, the expression of trehalase was nullified and no cointegration events of TPSP and RNAi transgenes were observed. However, trehalase activity was not significatively decreased. Until a few years ago, it was believed that very few plants, mainly those tolerant of desiccation after resuscitation after rehydration, were considered as producers of trehalose and even so in small quantities. Today, it is known that the apparent lack of

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trehalose in many species and its low concentration in others is due to the enzyme trehalase, which actively catalyzes the hydrolysis of trehalose in two glucose molecules (Wingler, 2002). In the metabolism of sugarcane disaccharides in normal environmental conditions, Glassop et al. (2007) found that trehalose and raffinose appear at concentrations that can be correlated with those of sucrose. T6P has been involved in the redox activation of ADP-glucose phosphorylase, the enzyme that catalyzes the first step of starch biosynthesis. In addition, T6P has been recognized as a key molecule that improves photosynthesis capacity. It has also been considered as a regulating molecule of the sugar influx and its metabolism since it inhibits hexokinase, thus regulating the entry of glucose and fructose in the glycolytic pathway (Grennan, 2007). In addition, a supply of exogenous trehalose increases the activity of ADP-glucose pyrophosphorylase and starch accumulation in Arabidopsis buds. As mentioned above, T6P has a profound influence on plant metabolism, growth, and development. Based on the experimental results obtained, T6P has been proposed to act as a signal of sugar availability by controlling sucrose accumulation. When Arabidopsis thaliana, deprived of carbon sources, were supplied with exogenous sucrose, the concentration of T6P significantly increased; same was also observed when they were supplied with hexose as long as they could be efficiently transformed into sucrose by the plants. This increase in T6P concentration was completely offset by a simultaneous treatment with cycloheximide, indicating that the accumulation process of T6P induced by sucrose is due to de novo synthesis of T6PS (Yadav et al., 2014). T6P is, therefore, both a positive signal for sucrose production and a negative feedback regulator of sugar levels in plants. That is, the increase in the production of active sucrose activates the TPS1 gene, responsible for the production of T6P and, simultaneously, represses the TPS2 gene, responsible for the synthesis of T6P phosphatase. Thus, T6P levels rise in concomitance with the increase of accumulated sucrose. But, in turn, high levels of T6P would suppress the SPS and SPP gene expression so that once the highest level of T6P is reached, sucrose production would automatically begin to decrease. This decrease would activate the T6PP gene, so that T6P levels would begin to decrease when trehalose is produced. Thus, the sucrose synthesis genes would be reactivated, and the process would begin anew (Figueroa and Lunn, 2016). This is a delicate loop of homeostatic regulation that tries to maintain the right levels of sucrose in the plant.

11.8 Conclusions and future prospects Different environmental factors, in extreme conditions, have a negative influence on the physiology of plants. In the specific case of sugarcane, due to its preferentially tropical nature, the stress caused by extreme temperatures, nutritional deficits, salinity, or drought causes serious disturbances in the physiology of the plant. Growth is negatively affected, as similarly the germination of its seeds. The leaves often suffer from chlorosis and the photosynthetic efficiency declines. Internal membrane systems can suffer irreversible disruptions due to oxidases and lipoxygenases that use ROS, whose accumulation is favored by stress.

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References

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Many genes involved in the resistance of sugarcane to stress have been identified and characterized. Some of them have been successfully cloned and incorporated into the genome of other species, such as A. thaliana and Nicotiana tabacum. In this way, transgenic plants have been able to successfully express these genes, demonstrating the resistance acquired through transformation. This clearly indicates that sugarcane cultivars, which are sensitive to different stresses, can be genetically transformed by means of similar techniques, thus allowing their agricultural use in extreme environmental conditions.

References Alexander, A., 1967. High sucrose levels and abnormal enzyme activity as a function of nutritional stress in sugarcane. J. Agric. Univ. Puerto Rico 51, 325 333. Alexander, A.G., 1968. In vitro effects of silicon on the action patterns of sugarcane acid invertase. J. Agric. Univ. Puerto Rico 52, 311 322. Begcy, K., Mariano, E.D., Gentile, A., Lembke, C.G., Zingaretti, S.M., Souza, G.M., et al., 2012. A novel stressinduced sugarcane gene confers tolerance to drought, salt and oxidative stress in transgenic tobacco plants. PLoS One 7 (9), e44697. Available from: https://doi.org/10.1371/journal.pone.0044697. Bruijn, J., 1970. Enzymatic hydrolysis of the polysaccharides formed by sugarcane after harvesting. Intern. Sugar J. 72, 1951 1958. Camargo, M.S., Bezerra, B.K.L., Vitti, A.C., Silva, M.A., Oliveira, A.L., 2017. Silicon fertilization reduces the deleterious effects of water deficit in sugarcane. J. Soil Sci. Plant Nutr. 17, 99 111. Cheong, Y.W., Heitz, Y.A., Deville, J., 1971. The effect of silicon on enzyme activity in vitro and sucrose production in sugarcane leaves. ISSCT 14, 777 785. Covacevich, M.T., Richards, G.N., 1977. Studies on dextrans isolated from raw sugar manufactured from deteriorated cane. Part I. Isolation, purification and structure of dextrans. Intern. Sugar J. 79, 3 9. Cox, M., Hogarth, M., Smith, G., 2000. Cane breeding and improvement. In: Hogart, H., Allsopp, P. (Eds.), Manual of Cane Growing. Bureau of Sugar Experimental Stations, Indooroopilly, pp. 91 108. Daniels, J., Roach, B.T., 1987. Taxonomy and evolution. In: Heinz, D.J. (Ed.), Sugarcane Improvement Through Breeding., vol. 11. Elsevier, Amsterdam, pp. 7 84. de Andrade, L.M., Brito, M.S., Peixoto, R.F., Marchiori, P.E.R., Paula Macedo No´bile, P.M., Martins, A.P.B., et al., 2017. Reference genes for normalization of qPCR assays in sugarcane plants under water deficit. Plant Methods 13, 28. Available from: https://doi.org/10.1186/s13007-017-0178-2. Eggleston, G., Legendre, B., Tew, T., 2004. Indicators of freeze-damaged sugarcane varieties which can predict processing problems. Food Chem. 87, 119 133. Figueroa, C.M., Lunn, J.E., 2016. A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiol. 172, 7 27. Fontaniella, B., Millanes, A.M., Pin˜o´n, D., Rodrı´guez, C.W., Vicente, C., Legaz, M.E., 2003. Effect of leaf scald on the content of sucrose and polysaccharides of two sugar cane cultivars. Food Sci. Biotechnol. 12, 346 350. Garcia, A.B., Engler, J., Iyer, S., Gerats, T., VanMontagu, M., Caplan, A.B., 1997. Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol. 115, 159 169. Glassop, D., Roessner, U., Bacic, A., Bonnett, G.D., 2007. Changes in the sugarcane metabolome with stem development. Are they related to sucrose accumulation? Plant Cell Physiol. 48, 573 584. Grennan, A.K., 2007. The role of trehalose biosynthesis in plants. Plant Physiol. 144, 3 5. Huang, Y.L., Yang, S., Long, G.X., Zhao, Z.K., Li, X.F., Gu, M.H., 2016. Manganese toxicity in sugarcane plantlets grown on acidic soils of Southern China. PLoS One 11 (3), e0148956. Available from: https://doi.org/10.1371/ journal.pone.0148956. Iskandar, H.M., Casu, R.E., Fletcher, A.T., Schmidt, S., Xu, J., Maclean, D.J., et al., 2011. Identification of droughtresponse genes and a study of their expression during sucrose accumulation and water deficit in sugarcane culms. BMC Plant Biol. 11, 12. Available from: http://www.biomedcentral.com/1471-2229/11/12. Julien, M.H.R., Irvine, J.E., Benda, G.T.A., 1988. Sugarcane anatomy, morphology and physiology. In: Ricaud, C., Began, B.T., Gillaspie, A.G., Hughes, C.G. (Eds.), Diseases of Sugarcane. Major Diseases. Elsevier, Amsterdam, pp. 1 19.

Plant Life under Changing Environment

268

11. Effects of abiotic stresses on sugarcane plants

Karpe, A., Nikam, A.A., Chimote, K.P., Kalwade, S.B., Kawar, P.G., Babu, H., et al., 2012. Differential responses to salinity stress of two varieties (CoC 671 and Co 86032) of sugarcane (Saccharum officinarum L.). Afr. J. Biotechnol. 11, 9028 9035. Legaz, M.E., Martı´n, L., Pedrosa, M.M., Vicente, C., de Armas, R., Martı´nez, M., et al., 1990. Purification and partial characterization of a fructanase which hydrolyzes natural polysaccharides from sugarcane juice. Plant Physiol. 92, 679 683. Legaz, M.E., de Armas, R., Martı´nez, M., Medina, I., Vicente, C., 1991. Binding studies of Mn21 to a glycosidase system from sugarcane juice. Plant Physiol. Biochem. 29, 601 605. Legaz, M.E., de Armas, R., Millanes, A.M., Rodriguez, C.W., Vicente, C., 2005. Heterofructans and heterofructancontaining glycoproteins from sugarcane: Structure and function. Recent Res. Devel. Biochem. 6, 31 51. Legaz, M.E., Pedrosa, M.M., Martı´nez, M., Vicente, C., 1995. Soluble glycoproteins from sugar cane juice analyzed by SEHPLC and fluorescence emission. J. Chromatogr. 697, 329 335. Legaz, M.E., Vicente, C., de Armas, R., 1998. Polyamines and phenols in commercial sugar preparations. Intern. Sugar J. 100, 433 436. Legaz, M.E., Blanch, M., Pin˜o´n, D., Santiago, R., Fontaniella, B., Blanco, Y., et al., 2011. Sugar cane glycoproteins may act as signals for the production of xanthan in the plant-associated bacterium Xanthomonas albilineans. Plant Signal. Behav. 6, 1132 1139. Legaz, M.E., Pedrosa, M.M., de Armas, R., Rodrı´guez, C.W., de los Rı´os, V., Vicente, C., 1998. Separation of soluble glycoproteins from sugarcane juice by capillary electrophoresis. Anal. Chim. Acta 372, 201 208. Legaz, M.E., Sa´nchez-Elordi, E., Santiago, R., de Armas, R., Fontaniella, B., Millanes, A.M., et al., 2018. Metabolic responses of sugar cane plants upon different plant pathogen interactions. In: Parvaiz Ahmad, P., Mohammad AbassAhanger, M.A., Singh, V.P., Tripathi, D.K., Alam, P., Mohammed Nasser Alyemeni, M.N. (Eds.), Plant Metabolites and Regulation Under Environmental Stress. Elsevier, Srinagar, in press. Martı´nez, M., Legaz, M.E., Paneque, M., de Armas, R., Pedrosa, M.M., Medina, I., et al., 1990a. The origin of soluble fructans in sugar cane juice. Intern. Sugar J. 92, 155 159. Martı´nez, M., Legaz, M.E., Paneque, M., Domech, R., de Armas, R., Medina, I., et al., 1990b. Glycosidase activities and polysaccharide accumulation in sugar cane stalks during post-collection impairment. Plant Sci. 72, 193 198. Medeiros, M.J.L., Silva, M.M.A., Granja, M.M.C., Souza, E., Silva, G., Camara, T., et al., 2015. Effect of exogenous proline in two sugarcane genotypes grown in vitro under salt stress. Acta Biol. Colom. 20, 57 63. Merlot, S., Gosti, F., Guerrier, D., Vavasseur, A., Giraudat, J., 2001. The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J. 25, 295 303. Minibayeva, F., Kolesnikov, O., Chasov, A., Beckett, R.P., Lu¨thje, S., Vylegzhanina, N., et al., 2009. Woundinduced apoplastic peroxidase activities: their roles in the production and detoxification of reactive oxygen species. Plant Cell Environ. 32, 497 508. Ngamhui, N.O., Akkasaeng, C., Zhu, Y.J., Tantisuwichwong, N., Roytrakul, S., Taksina Sansayawichai, T., 2012. Differentially expressed proteins in sugarcane leaves in response to water deficit stress. Plant Omics J. 5, 365 371. Nogueira, F.T.S., De Rosa, V.E., Menossi, M., Ulian, E.C., Arruda, P., 2003. RNA expression profiles and data mining of sugarcane response to low temperature. Plant Physiol. 132, 1811 1824. O’Neill, B.P., Purnell, M.P., Nielsen, L.K., Brumbley, S.M., 2012. RNAi-mediated abrogation of trehalase expression does not affect trehalase activity in sugarcane. Springer Plus 1, 74. Available from: http://www.springerplus.com/ content/1/1/74. Park, J.-W., Benatti, T.R., Marconi, T., Yu, Q., Solis-Gracia, N., Mora, V., et al., 2015. Cold responsive gene expression profiling of sugarcane and Saccharum spontaneum with functional analysis of a cold inducible Saccharum homolog of NOD26-like intrinsic protein to salt and water stress. PLoS One 10, e0125810. Available from: https://doi.org/10.1371/journal.pone.0125810. Passamani, L.Z., Barbosa, R.R., Reis, R.S., Heringer, A.S., Rangel, P.L., Santa-Catarina, C., et al., 2017. Salt stress induces changes in the proteomic profile of micropropagated sugarcane shoots. PLoS One 12 (4), e0176076. Available from: https://doi.org/10.1371/journal.pone.0176076. Roberts, E.J., Clarke, M.A., Godshall, M.A., Parris, F.W., 1985. A glucan from sugar cane. Intern. Sugar J. 87, 227 231.

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Further reading

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Rodriguez, C.W., Valdes, P., Martinez, M., 1985. Formacio´n de polisaca´ridos solubles de alto peso molecular en distintas variedades de can˜a de azu´car. Cienc. Agrar. 22, 63 68. Sa´nchez-Elordi, E., Baluˇska, F., Echevarrı´a, C., Vicente, C., Legaz, M.E., 2016. Defence sugar cane glycoproteins disorganize microtubules and prevent nuclear polarization and germination of Sporisorium scitamineum teliospores. J. Plant. Physiol. 200, 111 123. Sa´nchez-Elordi, E., Blanch, M., Vicente, C., Legaz, M.E., 2017. Interferences of sugarcane glycoproteins on the formation of commercial sucrose crystals. Adv. Food Sci. Eng. 1, 164 174. Shomeili, M., Nabipour, M., Meskarbashee, M., Memari, H.R., 2011. Evaluation of sugarcane (Saccharum officinarum L.) somaclonals tolerance to salinity via in vitro and in vivo. Hayati J. Biosci. 18, 91 96. Soares Netto, L.E., 2001. Oxidative stress response in sugarcane. Gen. Mol. Biol. 24, 93 102. Tang, S.Y., Li, Y.R., Yang, L.T., 2015. Evaluation of cold tolerance and photosynthetic characteristics in different sugarcane genotypes. J. Global Biosci. 4, 2459 2467. Thiebaut, F., Rojas, C.A., Almeida, K.L., Grativol, C., Domiciano, G.C., Lamb, C.R.C., et al., 2012. Regulation of miR319 during cold stress in sugarcane. Plant Cell Environ. 35, 502 512. Valdes, P., Rodriguez, C.W., 1982a. Formacio´n de polisaca´ridos en tallos de can˜a de azu´car recie´n cortados. Cienc. Agrar. 12, 45 52. Valdes, P., Rodriguez, C.W., 1982b. Respuestas de los tallos de la can˜a de azu´car a los cortes. Cienc. Agrar. 12, 118 122. Vantini, J.S., Carlin, S.D., Gimenez, D.F.J., Perecin, D., Ferro, J.A., Ferro, M.I.T., 2016. Proline accumulation in sugarcane roots subjected to drought conditions. Jaboticabal 44, 592 598. Vicente, C., Fontaniella, B., Legaz, M.E., 2000. Fructan-like polysaccharides produced by sugar beet during deterioration. Intern. Sugar J. 102, 250 256. Vu, J.C.V., Allen, L.H., 2009. Growth at elevated CO2 delays the adverse effects of drought stress on leaf photosynthesis of the C4 sugarcane. J. Plant Physiol. 166, 107 116. Wang, J., Nayak, S., Koch, K., Ming, R., 2013. Carbon partitioning in sugarcane (Saccharum species). Front. Plant Sci. 4. Available from: https://doi.org/10.3389/fpls.2013.00201. Wang, J., Zhao, T., Yang, B., Zhang, S., 2017. Sucrose metabolism and regulation in sugarcane. J. Plant Physiol. Pathol. 5, 4. Available from: https://doi.org/10.4172/2329-955X.1000167. Watanabe, K., Nakabaru, M., Taira, E., Ueno, M., Kawamitsu, Y., 2016. Relationships between nutrients and sucrose concentrations in sugarcane juice and use of juice analysis for nutrient diagnosis in Japan. Plant Prod. Sci. 19, 215 222. Wingler, A., 2002. The function of trehalose biosynthesis in plants. Phytochemistry 60, 437 440. Yadav, U.P., Ivakov, A., Fei, R., Duan, G.Y., Walther, D., Giavalisco, P., et al., 2014. The sucrose trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J. Exp. Bot. 65, 1051 1068. Yang, Y., Zhang, X., Su, Y., Zou, J., Wang, Z., Xu, L., et al., 2017. miRNA alteration is an important mechanism in sugarcane response to low temperature environment. BMC Genomics 18, 833. Available from: https://doi. org/10.1186/s12864-017-4231-3. Zeng, Q., Ling, Q., Fan, L., Li, Y., Hu, F., Chen, J., et al., 2015. Transcriptome profiling of sugarcane roots in response to low potassium stress. PLoS One. Available from: https://doi.org/10.1371/journal.pone.0126306.

Further reading Abbas, S.R., Gardazi, S.D.A., Sabir, S.M., Batool, A., Rao, A., Shah, A.H., et al., 2013. Measurement of lipid peroxidation and phenol contents under heat stress condition in sugarcane genotypes. J. Agric. Sci. 5, 214 220. Gilani, S., Wahid, A., Ashraf, M., Arshad, M., 2008. Changes in growth and leaf water status of sugarcane (Saccharum officinarum) during heat stress and recovery. Int. J. Agric. Biol. 10, 191 195. Gomathi, R., Shiyamala, S., Vasantha, S., Johnson, D.E., Janani, P.K., 2013. Kinetics of metabolism in sugarcane (Saccharum officinarum L.) under heat stress. Ind. J. Plant Physiol. 18, 41 47. Murad, A.M., Molinari, H.B.C., Magalhaes, B.S., Franco, A.C., Takahashi, F.S.C., Gomes de Oliveira, N., et al., 2014. Physiological and proteomic analyses of Saccharum spp. grown under salt stress. PLoS One 9, e98463. Available from: https://doi.org/10.1371/journal.pone.0098463. Zingaretti, S.M., Rodriguez, F.A., da Grac¸a, J.P., Pereira, L.M., Lourenc¸o, M.V., 2012. Sugarcane responses at water deficit conditions. In: Rahman, I.M.M. (Ed.), Water Stress. In Tech Europe, Rijeka, Croatia, pp. 255 276.

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C H A P T E R

12 Heavy metal stress and plant life: uptake mechanisms, toxicity, and alleviation Swati Singh1, Vaishali Yadav1, Namira Arif1, Vijay Pratap Singh2, Nawal Kishore Dubey3, Naleeni Ramawat4, Rajendra Prasad5, Shivendra Sahi6, Durgesh Kumar Tripathi4 and Devendra Kumar Chauhan1 1

D D Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Prayagraj, India 2Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, India 3Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, India 4Amity Institute of Organic Agriculture, Amity University Uttar Pradesh, Noida, India 5Department of Horticulture, Kulbhaskar Ashram Post Graduate College, Prayagraj, India 6University of the Sciences in Philadelphia (USP), Philadelphia, PA, United States

12.1 Introduction Heavy metals (HMs) pollution in environment occurs due to their release from natural resources such as rocks, ore minerals, volcanoes, and weathering (Szyczewski et al., 2009) and various anthropogenic activities such as urban advancement, electricity generation, and mining and refinery industries (Kabata-Pendias and Mukherjee, 2007; Norgate et al., 2007). HMs are transition metals, which possess atomic masses more than 0.002 kg, weight about 5 N/m3, and density greater than 5 g/cm3 (Ja¨rup, 2003; Rascio and Navari-Izzo, 2011). These metals are categorized as essential metals such as copper (Cu), zinc (Zn),

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manganese (Mn), nickel (Ni), iron (Fe), cobalt (Co), molybdenum (Mo), and selenium (Se) and nonessential metals. Essential HMs play vital regulatory roles in several cellular reactions including electron transfer and in enzyme activation, in redox reaction as well as in the synthesis of pigments (Babula et al., 2009; Fageria et al., 2009; Chaffai and Koyama, 2011), whereas nonessential metals, such as chromium (Cr), cadmium (Cd), lead (Pb), silver (Ag), mercury (Hg), and arsenic (As), have no role in any biological reaction and cause toxic impacts even at low concentrations by competing with crucial elements at proteinbinding sites (Torres et al., 2008). Although when the amount of these metals increases beyond the optimum point, they cause toxicity in plants by decreasing growth, causing soil quality deterioration as well as affecting the yield with probable health effects on plants (Seth et al., 2007; Seth, 2012). Toxicity of HMs depends on the concentration, reactivity as well as their oxidation capacity (Szyczewski et al., 2009). Crops are more susceptible to these HMs, and they transport to organism through the food chain. HM-stressed plant shows alteration in cellular mechanisms and gene regulation (Hussain et al., 2004; Chaffai and Koyama, 2011; Choppala et al., 2014). These HMs generate free radicals in cells, which further cause toxicity in plants. Nonessential metals slow down the various physiological reactions through the alteration in biomolecules and in regulatory proteins or by replacement of crucial metals (Sarwar et al., 2010) as well as disturb the integrity of biomolecules and affect antioxidant defense system by generating reactive oxygen species (ROS) (Sarwar et al., 2010; Chaffai and Koyama, 2011; Choppala et al., 2014) (Fig. 12.2). Plant acquires several defense approaches to safeguard against metal toxicity such as sequestration, compartmentalization, exclusion, and inactivation by the secretion of organic ligands (Choppala et al., 2014). Besides this, plants also induce antioxidant system as well as maintain the metal homeostasis by restricting the metal bioavailability. Cadmium (Cd) is categorized as a toxic HM that contaminates the agricultural and mining industries (Foy et al., 1978). It naturally presents in the environment such as in soil with an average value more than 1 mg K/g (Peterson and Alloway, 1979). Chlorosis, leaf rolls, and stunting growth of plants are the usual symptoms of cadmium toxicity (Table 12.1). Cadmium caused harmful impacts on plant productivity and development by affecting stomatal opening, transpiration, and photosynthesis (Gabrielli and Sanita` di Toppi, 1999) (Fig. 12.1). It also decreased the nitrate absorption and transportation from root cell to stem shoot by reducing the activity of nitrate reductase in the shoot (Hernandez et al., 1996). It also alters the permeability of plasma membrane and reduces the water conduction (Barcelo et al., 1986; Poschenrieder et al., 1989; Costa and Morel, 1994) (Fig. 12.1). Chromium is in the list of most commonly occurring elements in the earth. Cr is an important industrial pollutant that is found in two oxidation forms: Cr(III) and Cr(VI). Cr(III) is insoluble and less mobile, whereas Cr(VI) being highly soluble and easily available to plants (Cary, 1982). Chromate is easily transported across the plasma membrane, and when it enters the cell, it reduces to Cr(III). These forms are highly toxic to plants and cause negative impacts on plant growth and development (Shanker et al., 2005). Due to chromium toxicity, plant shows stunted growth, wilting of tops, chlorosis as well as damage of root and shoot (Sharma et al., 2003) (Table 12.1). Chromium causes ultrastructural changes in the thylakoid, which leads to reduction in photosynthesis (Ali et al., 2013) (Fig. 12.1). Copper is an essential nutrient for the plant, and its concentration is low that is about 20 30 ppm in normal soils and sediments (Nriagu, 1979; Salomonsand and Fo¨rstner, 2012) and

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TABLE 12.1

Negative impacts of deferent heavy metals on plants.

Heavy metals

Plant

Negative impacts on plant

References

As

Brassica

Decreased plant growth as well as affected the root vascular cylinder diameter and the height of epidermal cell

de Freitas-Silva et al. (2016)

Rice

Deformed root anatomy and caused lower root-specific surface area

Deng et al. (2010)

Mung bean

Cause reduction in root elongation by inducing oxidative stress Singh et al. (2007) due to enhanced lipid peroxidation but not H2O2 accumulation

Cd

Cu

Common bean Induced growth inhibition associated with anomalies in anatomical structure, reduction in pigment composition, increased level of reactive oxygen species, and also affected the antioxidant enzyme

Talukdar (2013)

Avicennia marina

Cadmium mainly accumulated in the root, caused anatomical changes such as decreased cross-sectional area of xylem and the central cylinder area and decreased width of epidermis

Zhang et al. (2013)

Brassica juncea

Caused structural changes in root, stem, and leaf, altered physiological and morphological characteristics

Sridhar et al. (2005)

Merwilla plumbea

Toxicity resulted in hypodermal periderm development in young root part and also the protective suberized layer

Lux et al. (2010)

Arachis hypogaea

Inhibition in net photosynthetic rate as well as reduction in stomatal conductance and altered leaf structure, decrease in transpiration rate

Shi and Cai. (2008)

Origanum vulgare

Cause anatomical changes such as disrupted epidermis, cortex of large cells with folded walls

Panou-Filotheou and Bosabalidis. (2004)

Cytological alterations occurred such as metamorphosis of the amyloplast

Cr

Myriophyllum alterniflorum

Differentially affected physiological parameters such as pigment contents, osmotic potential, and proline content cell and influence membrane integrity of young leaf under increased MDA content

Delmail et al. (2011)

Bean

Showed modification in the cell wall of various tissues such as abnormal cell wall thickening in endodermis, reduction in the water absorption by plant, enhanced phenylalanine ammonia lyase

Bouazizi et al. (2010)

Bruguiera sexangula

Percolated hypodermal and stealer region, xylem and phloem deformation

Gupta and Chakrabarti. (2013)

Rice

Decreased length of epidermis and stomatal frequency, adversely affecting chloroplast as well as deformed integrity of xylem and phloem, decreased plant growth, photosynthetic pigment, and protein

Tripathi et al. (2012)

Phaseolus vulgaris

Reduced germination percentage, radicle growth as well as plant growth and photosynthetic pigment

Zeid (2001) (Continued)

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TABLE 12.1 (Continued) Heavy metals

Fe

Plant

Negative impacts on plant

References

Mentha aquatica

Collapsed root cap and statolith, loss of tissue organization, increase in intercellular spaces in mesophyll, less development of chloroplast and starch granules

Bianchi et al. (1998)

B. juncea

Causes growth retardation, reduced number of palisade and spongy parenchyma, clotted deposition of vascular bundles, increased number of vacuoles along the vascular bundle

Han et al. (2004)

Canavalia rosea Altered nutrient uptake, changed external morphology of lateral root, deformed pericycle and cortex

Siqueira-Silva et al. (2012)

Ipomoea batatas Reduced stomatal density, radicle cell showed mitochondrial impairment, decreased nutrient uptake, and increase in antioxidative enzymatic activities

Adamski et al. (2012)

MDA, Malondialdehyde.

FIGURE 12.1

Source and toxicity of heavy metals.

below 2 ppb in natural waters (Baccini, 1985). But at higher concentration, it causes detrimental impacts on plant tissue and plant physiology and biochemistry such as disturbance in fatty acids and protein metabolism as well as inhibition in respiration and nitrogen fixation (Table 12.1). Iron (Fe) is the fourth recorded abundant metal in the Earth’s crust, which usually presents in well-aerated soil in the Fe31 and Fe21 forms. It works as an electron acceptor and donor in the various electron transport chains of photosynthesis and

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respiration (Fig. 12.1). It also acts as a limiting factor for the biomass production. Arsenic (As) is toxic metalloid and broadly disseminated in the environment, it predominately occurs in the form of As(V) and As(III) (Tripathi et al., 2007). At higher concentration, both forms interact with the metabolic processes and inhibit the plant growth, which leads to plant death (Table 12.1). Arsenic disturbs the chloroplast membrane and also affects the photosynthetic mechanism (Stoeva and Bineva, 2003) (Table 12.1). It also interferes with nutrient homeostasis by competing with the essential element (Meharg and Macnair, 1990; Garg and Singla, 2011) (Fig. 12.1).

12.2 Sources and metal bioavailability HMs enter the environment by natural as well as anthropogenic activities and transport over long distance in agro-ecosystem (Shahid et al., 2015; Saher and Siddiqui, 2016). HMs discharge naturally in the environment via the natural process (Szyczewski et al., 2009). Several anthropogenic activities are responsible for HMs that contaminate soil, air, and water, and these origins reach up to several times more than the natural emissions (Chmielewska and Spiegel, 2003). These anthropogenic activities having industrial activities such as sewage, mining and waste processing (Kabata-Pendias and Pendias, 1984; Tanhan et al., 2007), commercial fertilizers, power units, and several developmental industries (Wu et al., 2004). Due to these anthropogenic activities, HMs increase in the environment, cause serious threat to food security for the growing world population (Ayangbenro and Babalola, 2017), and also have detrimental impacts on ecosystems (Harguinteguy et al., 2016). Nowadays, mineral sources, abstraction, and utilization of various minerals in several industrial processes have imposed threats in the form of HM pollution (Li et al., 2014; Goix et al., 2015; Niazi and Burton, 2016). Numerous cases of atmospheric contamination such as release of persistent and harmful HMs that were absorbed by the atmospheric dust particles, organic pollutants, and biodegradation are the main sources of HMs in the environment (Norouzi et al., 2016). The absorption of HMs depends mainly upon the availability of these metals regulated through the different factors (Benavides et al., 2005). Metals retain in the soil in the form of various chemicals in equilibrium due to soil properties (Chaney, 1988). Solis have HMs mostly in three forms: by absorption from mineral particles, through the complexation with humus or via the precipitation reactions. Only a small amount of metal is sufficient for the plant uptake (Walton, 1994). Usually the soil metal bulks are not available for transport into the roots (Lasat, 2002). Plants acquire extremely specific route to arouse metal availability in the soil as well as to increase absorption into the root cells (Ro¨mheld and Marschner, 1986). The significant roles of root exudates have been reported in the attainment of various nutrient metals. For instance, some grasses have been of roots exudates organic acids (OAs), that are known as siderophores such as mugineic and avenic acids, which considerably enhance the soil-bound iron bioavailability (Kanazawa et al., 1994) and possibly zinc (Cakmak, 1996a,b). Though in dicot iron acquisition is facilitated through the acidification of rhizosphere via the efflux of H1 ion from roots, but due to acidic environment, ferric iron reduces to ferrous that is easily absorbed through the plant cell (Chaney et al., 1972; Bienfait et al., 1982). Metal availability also causes impact on the plant and microbial activities. Some bacterial sp. release biosurfactants such as

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rhamnolipids, which make hydro-labile pollutants more soluble in water (Volkering et al., 1997). Plant also releases some lipophilic compounds that are known for increasing pollutant solubility or they can also promote microbial populations that are able to produce biosurfactants (Siciliano and Germida, 1998). Availability of metals affected by the metal chelators such as siderophores, OAs, and phenolics released by the plant and bacterial cells that liberate metal ions from soil and make the metals easily available to them (Pilon-Smits, 2005).

12.3 Consequences of heavy metals in plants HMs affect the environment in several ways on different levels. It influences the organisms both positively and negatively depending on the type of metals and its concentration. On the positive aspect, HMs serve as essential micronutrients; and on negative aspect, it induces the severe toxicity (Kafka and Puncocharova, 2002). Similarly, in the plants, toxic HMs may lead to chlorosis, necrosis, phenotypic changes, and damage to plant organs (Benzarti et al., 2008). Moreover, they potentially affect physiology and biochemical structure of plant and could also hinder the growth parameters and ultimately the cell death in the plant (Popova et al., 2009). The growth reduction occurs due to decrease in photosynthetic rate, chlorophyll content, and breakage of cellular membranes. Moreover, alteration in the cell molecules and organelles occurs by the generation of ROS (Ekmekc¸i et al., 2009). Metal phytotoxicity increased oxidative stress that causes toxicity and affects antioxidant defense system. Burst of free radicals in plant cell is a stress marker, but these reactive radicals also behave as a messenger in signaling (Pourrut et al., 2013). HMs in contact with plants cause an inequity between ROS generation and their removal, therefore physiological changes occur (Jonak et al., 2004). HM-induced overgeneration of ROS, which leads to apoptosis as a result of which membrane peroxidation, damage to RNA, DNA, and key enzymes inhibition, and protein oxidation occur in plants (Flora, 2011; Shahid et al., 2014). Therefore to prevent their damage to cells caused by HMs plant established a defense mechanism with the help of phytochelatins (PCs), metallothioneins (MTs), and sulfur compounds (Hossain et al., 2012). The cell defense system of plant consists of both nonenzymatic system; glutathione (GSH), ascorbic acid (AA), a-tocopherol, b-carotene, and enzymatic system; superoxide dismutases, catalases, peroxidases, GSH reductases, and NADP1-reducing enzymes (Hossain et al., 2012). Plants generate ROS naturally in various organelles such as chloroplasts, mitochondria, and peroxisomes (Shahid et al., 2014). These radicals are highly reactive, unstable and possess free electrons in their last shell. Hydrogen peroxide (H2O2), singlet oxygen (1O2),    superoxide anion (O2 2 ), hydroxyl (HO ), alkoxyl (RO ), peroxyl (RO2 ) radicals, and organic hydroperoxide (ROOH) are ROS, and their generation increase in the plant tissue due to HM toxicity (Shahid et al., 2017). HMs reduced the plant growth by affecting the photosynthetic activity and photosynthetic pigments (Sheoran and Singh, 1993). Metals also cause water stress by affecting stomatal and transpiration activity, relative water content in leaf due to decrease in size and quantity of xylem tissue, chloroplast, and cell elongation. These metals enter the food chain via edible plant parts so it is necessary to eliminate the HMs from the ecosystem in order to regulate a healthy environment (Adrees et al., 2015).

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12.4 Mechanisms of heavy metals uptake and transport in plants The absorption of HMs in plant tissue is mediated at the extracellular and intracellular levels through the mixed reaction of physiological, biochemical, and molecular mechanisms in polluted soils (Hossain et al., 2012). Internally plants distribute metals in several distinct ways. These HMs are either localized in root and stem or accumulated in different parts in the nontoxic forms for further distributions and use. In plants, HMs are uptakes by the cortical cells of the root by the competitive uptake with vital elements and follow the symplastic and apoplastic pathways (Salt et al., 1995). The movement of metal to the root surface mainly depends on these following factors: mass flow, that is, metal ions absorbed by the root surface, through the diffusion mechanism as well as by the root interception cause by root growth (Anjum et al., 2012). The uptake of metal may be through the apical region of the root or through the entire surface depending upon the respective metals. In addition, metal uptake also depends upon the root capacity and growth. There are two ways for the entrance of HMs to plant cell, these are apoplastic (extracellular) and symplastic (intracellular) routes. Apoplastic way of the root is easily permeable to solutes, where metals are absorbed in the root cell walls due to their negatively charged sites (Lasat, 2002) and translocate into the root tissue, whereas the suberin lamellae prevent the solutes from the apoplast to xylem (Taiz and Zeiger, 2002). Metal ions transport through the protein for their further translocation from endodermis to xylem of root (Pilon-Smits, 2005). Some HMs are chelated through the OAs (Kra¨mer et al., 1996). But it is unclear for some metals that how they chelate and which transport protein is responsible for their transportation into the root xylem (Pilon-Smits, 2005), because of their charged metal ions easily cannot across the lipophilic structure of cell walls. Thus cells must mediate ion transport by transporter protein (Lasat, 2002). Various transporters such as CPx-ATPases, the Nramps, and cation diffusion facilitator family (Williams et al., 2000), and ZIP family in plants are worked for metal uptake and homeostasis for the metal tolerance (Guerinot, 2000; Hall, 2002). Moreover, HM ions such as Cd enter the plant through the transporters for cations such as Fe21 (Thomine et al., 2000). Membrane transporter possesses an extracellular domain that binds the specific metals and a transmembrane domain that remain in extracellular and intracellular membrane mediums that transfer metal from outside to inside cell (Lasat, 2002). These transporters possess specific transport capacity (Vmax) and affinity for ion (Km) (Axelsen and Palmgren, 2001). Transportation of HMs from root to shoo occurs via the xylem by specific membrane transport mechanism. For instance, Ni loading in xylem tissue may be derived by the complexation of Nickel to free histidine (Salt et al., 1995; Kra¨mer et al., 1996). Translocation of metals in xylem tissue is mainly occurred through the transpirationdriven mass flow (Salt et al., 1995). The cell wall of xylem has high cation-exchange capacity (CEC), consequently noncationic metal chelate complexers should be moved effortlessly in xylem (Senden and Wolterbeek, 1990). Cadmium translocated into the xylem tissue through the chelation in the form of cadmium citrate, while PCs and other thiolcontaining ligands do not directly involve in cd transportations (Salt et al., 1995)

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(Table 12.1). The movement of metals in the xylem strands from the root cell to stem is mainly occurred through the transpiration, that is, to create a negative pressure to move water and solutes upward (Taiz and Zeiger, 2002), and in the leaf, metals are transported through the membrane transport proteins. Metals are transported by precise membrane transporter proteins, and when they are taken up by the symplast, compartmentalized in specific organelles, they could not be much harmful to essential cellular processes. Mainly these HMs are accumulated into the vacuole or cell wall (Burken, 2003; Cobbett and Goldsbrough, 2002), whereas in tissue HMs are gathered in the epidermal layer or hairs.

12.5 Mechanism of heavy metals detoxification/tolerance in plants Plants acquire several cellular mechanisms, including extracellular and intracellular, to avoid the metal toxicity. On the primary stage, root cells check the entry of metals by adopting avoidance strategy, but when somehow these metals enter the root cells, detoxified by several mechanisms such as cell wall binding, OAs, chelation, and sequestration, these intracellular detoxification mechanisms are called tolerance strategy of plants against the metal toxicity. Antioxidative defense systems as well as the formation of stress-related proteins in plants are also the part of tolerance mechanism in metal toxic plants. So the plant utilizes two types of strategies against the metal toxicity, avoidance (restriction to metal uptake) and tolerance (intracellular detoxification) (Dalvi and Bhalerao, 2013). These metals are sequestered in the leaf cell, bounded by the chelators. Chelators implicated in metal sequestration comprise the tripeptide glu-cys-gly (GSH) and its oligomer, the PCs and MTs show active role in sequestration, tolerance, and in regulation of vital metals (Goldsbrough, 2000).

12.6 Avoidance mechanisms Avoidance strategies limit the uptake of HMs and check the entry of metal ions into plant cells through the root tissues, these mechanisms are the first line of extracellular defense system against the metal toxicity. This extracellular defense system involves several strategies such as immobilization by mycorrhiza, complexation through root exudates, and alteration of rhizosphere pH, secretion of metal-binding OAs, or development of redox barrier (Fig. 12.2). Ectomycorrhizas and Arbuscular mycorrhiza are the mycorrhizal association, which grow on HM-polluted soil. Mycorrhizas acquired exhibits effective exclusion barriers such as absorption, adsorption, or chelation mechanisms to check the influx of HMs in to host plant (Dalvi and Bhalerao, 2013) (Fig. 12.2). Besides this, root also releases amino acids or OAs, water, inorganic ions, carbohydrates, etc. as well as excretes bicarbonates, protons, carbon dioxide, and secretes mucilage, siderophores, allelopathic compounds, etc. (Fig. 12.2), which are communally called root exudates and play an important role to survive the plant in polluted areas by forming stable ligand complexes and make the metals less toxic (Dalvi and Bhalerao, 2013). Cellular exclusion is an imperative adaptation strategy against the metals toxicity. Huge amount of metals in roots are mainly present in apoplastic space (Hossain et al., 2012).

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FIGURE 12.2 Mechanism of HM detoxification/tolerance in plants. HM, Heavy metals.

The cell wall and plasma membrane could be a potential site for the HM tolerance due to their accumulation properties such as Italian ryegrass (Lolium multiflorum), which accumulates about 60% of copper in the root cell wall and plasma membrane (Iwasaki et al., 1990). Plant CEC depends upon the exchange sites of roots cell wall (Horst and Marschner, 1978). Sensitive wheat cultivars have less cell wall CEC than tolerant cultivars (Masion and Bertsch, 1997), which shows the tolerant varieties have high CEC to prevent the entry of HMs (Hossain et al., 2012). Reichman (2002) had described about utilization strategy of plant to produce metal tolerance by active efflux that decreases the intracellular concentration to subtoxic levels.

12.7 Metal binding to cell wall Extracellular carbohydrates present in cell walls check the uptake of HMs in to the cytosol. Cell wall pectins contain polygalacturonic acid, which are cation exchangers and bound the HMs into their carboxyl group and prevent the uptake of HMs (Fig. 12.2). Several studies reported that metal tolerance influenced by the metal uptake, which is generally modulated by the chemical properties of the cell wall. On the other side the plant cell wall minimally influenced the HM tolerance because of lacking of sites of metal absorption. Therefore the complete mechanism of the plant cell wall against HMs toxicity is still not well understood and revealed (Dalvi and Bhalerao, 2013). Plants are capable of lessening the negative impacts of toxic HMs by controlling the metal allocation and localization within the cells. Besides hyperaccumulator, much higher

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amount of metals present in plants root in comparison to shoot to minimize the transportation and accretion of HMs to the cells of plant shoot (Hossain et al., 2012). So the tolerant genotypes have a lesser amount of HMs in the shoot than the sensitive genotypes. Therefore tolerant cowpea (Vigna unguiculata) genotypes have found homogenized allocation of Mn in the leaf thoroughly, while the nontolerant genotypes agglomerate Mn in the specific area of leaf in the form of dark brown spots of manganese oxide precipitates (Hossain et al., 2012).

12.8 Tolerance mechanisms HM tolerance mechanisms include accumulation, restoration, and immobilization of HMs as metals get bonded with the amino acids, proteins, or peptides and makes a complex. However, it is known as the “plant’s second line of defense,” which chiefly accelerates intracellular detoxification of metals in the plants. Furthermore, Tong et al. (2004) described that on toxicity of HMs, plants primarily bind or modify the metal ions to minimize the metal transport across the plasma membrane and which metal ions entered the plant cells were detoxified by their inactivation or converting them into less toxic forms (Dalvi and Bhalerao, 2013). Once an HM got entry in cells, plants acquire various strategies to cope with it, such as transporting of HMs out of the cells, sequestration of ions into the vacuole or other cell organelles where sensitive metabolic process occurs (Clemens, 2001). So the central vacuole is a suitable storage sites for toxic HMs accumulation, and the two vacuolar proton pumps, a vacuolar proton-ATPase and a vacuolar proton pyrophosphatase, facilitate the vacuolar up take of solutes, which are catalyzed by the channels or transporters. When these metals are sequestered in vacuoles they bind by chelators that are polypeptides. The two significant metal-binding polypeptides are found in plants such as MTs and PCs. MTs have significant properties, thereby regarded as gene-encoded, cysteine-rich polypeptides with low molecular weight (Robinson et al., 1993). Numerous MT genes (MT1, MT2, MT3, and MT4) now have also been found involved in different higher plants, including Arabidopsis (Goldsbrough, 2000). PCs are also class III MTs, which may be cysteine rich having general structure (3 -Glu Cys) n-Gly with n 5 2 11. PCs are produced from GSH by a specific transpeptidase named 3-glutamyl cysteine dipeptidyl transpeptidase, a phytochelatin synthase (PCS) (Vatamaniuk et al., 2004), required for posttranslational activation by the HMs (Klapheck et al., 1995). The best activator for the enzyme PCS is cadmium whereas moderately activate in the presence of silver, lead, zinc, etc. (Cobbett, 2000; Pickering et al., 2000). PCs sequestered the metal PC complexes in the cell vacuole via the tonoplast membrane through ABC transporter (Schat et al., 2002), further they stabilized by the acid-labile sulfide (Cobbett and Goldsbrough, 2002). These PCs play an imperative role in the exclusion of cadmium and arsenic, while playing an insignificant role in the alleviation of HMs such as Cu, Zn, Ni, and SeO3 (Cobbett, 2000). Hyperaccumulators possess extra mechanisms to detoxify metal for instance Ni hyperaccumulator—Thlaspi goesingense has high tolerance of Ni as it makes complex with the histidine, which further causes metal inactivation (Kra¨mer et al., 1996). At cytoplasmic level, PCs and MTs have significant role in the metal tolerance, by forming complexes with metals, and store these complexes into the vacuole without any negativity (Hall, 2002).

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HM tolerance and detoxification in plants occurs via two mechanisms: external and internal tolerance and detoxification. However, under external detoxification mechanism, it involves excretion of OAs from roots and forms a stable compound with metal ions and affects their mobility and bioavailability to the plants (Fig. 12.2). In the internal tolerance, chelation occurs through OAs into the cytosol or makes metal ions less toxic (Hall, 2002). Plants produce several potential ligands such as carboxylic and amino acids (AAs) for the tolerance of HM ions (Hall, 2002; Balaji et al., 2003; Yang et al., 2005; Sharma and Dietz, 2009; Singh and Chauhan, 2011; Sunitha et al., 2013). These acids within cells detoxify metals by forming stable compounds and make these metals unavailable to plants, and it also has role in nitrogen metabolism under which it acts as metabolic intermediates in the generation of ATP from carbohydrates. Consequently, metabolic anomaly in these mechanism reflected by the changes in the OA concentration. So the increase concentration of OAs at the metals toxicity could be detoxification mechanisms or consecutively irregularities in the metabolism produced OA as an indicator of metal stress (Dalvi and Bhalerao, 2013). Many researchers have been worked on the hyperaccumulator plants during the last few decades. Hyperaccumulation depends on the plant species, pH, organic matter content, CEC of the soil as well as the types of metals (Sarma, 2011). In hyperaccumulator plants, there is a fast and an efficient movement of metals from root to shoot by the xylem tissue, which could be driven by the transpiration (Salt et al., 1995). Hyperaccumulation of HMs occurs even at low external metal amount. HM uptake is tremendously high in hyperaccumulators in root tissues, because of highly active membrane transporter in the plasma membrane. These transporters tolerate metals stress via the process of intracellular compartmentalization and chelation (Pilon-Smits and Pilon, 2002). Several chelators such as OAs or nicotianamine also play a dynamic role in the transportation of metal ions through the xylem tissue (Sunitha et al., 2013). On metal exposure, plants synthesize various types of novel proteins in which most of the proteins play a regulatory role for HM influx in the plant that ultimately leads to the metal homeostasis and its exclusion. Heat shock proteins, which are stress related, act as “molecular chaperones” and work in posttranscriptional process. Moreover, it might also play an imperative role in the defacing and restoring of proteins under stressed condition. Increased generation of ROS is the primary indicator of HM-induced stress. At low level, during normal metabolic processes, these ROS constantly produce in the plant. Therefore hydrogen peroxide (H2O2) acts as a signaling messenger that modulates defense system. ROS have dual function: at the elevated concentration, they damage the tissue; while at normal level, they induce the antioxidant system. However, a decreased level of oxidative burst with increased resistivity to HMs occurs through the complex ROS destruction mechanism at the molecular and cellular levels. Peleg and Blumwald (2011) suggested that the increased synthesis of hormones due to HM toxicity shows the adaptation of plants. Hormones such as salicylic acid (SA), jasmonic acid (JA), ethylene, and gibberellic acid (GA) are involved in the plant defense signaling pathways. JA increased the biosynthesis of GSH and ethylene, which play an active role in the defense of HMs toxicity (Bajguz and Hayat, 2009). Besides this, vacuolar sequestration, morphological features of the plant perform an essential role in the sequestration of HMs thereby removes the induced toxicity (Fig. 12.2). Moreover, various

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12. Heavy metal stress and plant life: uptake mechanisms, toxicity, and alleviation

reported studies also discussed about the mechanism of metal mitigation through sequestration and chelation, and also the role of glandular trichomes and epidermal structures (hydropotes) in these processes.

References Adamski, J.M., Danieloski, R., Deuner, S., Braga, E.J., de Castro, L.A., Peters, J.A., 2012. Responses to excess iron in sweet potato: impacts on growth, enzyme activities, mineral concentrations, and anatomy. Acta Physiol. Plant. 34 (5), 1827 1836. Adrees, M., Ali, S., Rizwan, M., Zia-ur-Rehman, M., Ibrahim, M., Abbas, F., et al., 2015. Mechanisms of siliconmediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol. Environ. Saf. 119, 186 197. Ali, B., Tao, Q., Zhou, Y., Gill, R.A., Ali, S., Rafiq, M.T., et al., 2013. 5-Aminolevolinic acid mitigates the cadmiuminduced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. Ecotoxicol. Environ. Saf. 92, 271 280. Anjum, N.A., Pereira, M.E., Ahmad, I., Duarte, A.C., Umar, S., Khan, N.A., 2012. Phytotechnologies: Remediation of Environmental Contaminants. CRC Press. Axelsen, K.B., Palmgren, M.G., 2001. Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol. 126 (2), 696 706. Ayangbenro, A., Babalola, O., 2017. A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int. J. Environ. Res. Public Health 14 (1), 94. Babula, P., Adam, V., Opatrilova, R., Zehnalek, J., Havel, L., Kizek, R., 2009. Uncommon heavy metals, metalloids and their plant toxicity: a review. Organic Farming, Pest Control and Remediation of Soil Pollutants. Springer, Dordrecht, pp. 275 317. Baccini, P., 1985. Metal transport and metal/biota interactions in lakes. Environ. Technol. 6 (1 11), 327 334. Bajguz, A., Hayat, S., 2009. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol. Biochem. 47 (1), 1 8. Balaji, M., Krishna Reddy, B., Jogeswar, G., Ananda Reddy, L., Kavi Kishor, P.B., 2003. Alleviating effect of citrate on alluminium toxicity of rice (Oryza sativa L.) seedlings. Current Sci. 85, 383 386. Barcelo, J., Poschenrieder, C., Andreu, I., Gunse, B., 1986. Cadmium-induced decrease of water stress resistance in bush bean plants (Phaseolus vulgaris L. cv. Contender) I. Effects of Cd on water potential, relative water content, and cell wall elasticity. J. Plant Physiol. 125 (1 2), 17 25. Benavides, M.P., Gallego, S.M., Tomaro, M.L., 2005. Cadmium toxicity in plants. Braz. J. Plant Physiol. 17 (1), 21 34. Benzarti, S., Mohri, S., Ono, Y., 2008. Plant response to heavy metal toxicity: comparative study between the hyperaccumulator Thlaspi caerulescens (ecotype Ganges) and nonaccumulator plants: lettuce, radish, and alfalfa. Environ. Toxicol. 23 (5), 607 616. Bianchi, A., Corradi, M.G., Tirillini, B., Albasini, A., 1998. Effects of hexavalent chromium on Mentha aquatica L. J. Herbs Spices Med. Plants 5 (4), 3 12. Bienfait, H.F., Duivenvoorden, J., Verkerke, W., 1982. Ferric reduction by foots of chlorotic bean plants: indications for an enzymatic process. J. Plant Nutr. 5 (4 7), 451 456. Bouazizi, H., Jouili, H., Geitmann, A., El Ferjani, E., 2010. Copper toxicity in expanding leaves of Phaseolus vulgaris L.: antioxidant enzyme response and nutrient element uptake. Ecotoxicol. Environ. Saf. 73 (6), 1304 1308. Burken, J.G., 2003. Uptake and metabolism of organic compounds: green-liver model. Phytorem.: Transform. Control Contam. 59, 59 84. Cakmak, I., Sari, N., Marschner, H., Ekiz, H., Kalayci, M., Yilmaz, A., et al., 1996a. Phytosiderophore release in bread and durum wheat genotypes differing in zinc efficiency. Plant Soil 180 (2), 183 189. Cakmak, I., Yilmaz, A., Kalayci, M., Ekiz, H., Torun, B., Ereno, B., et al., 1996b. Zinc deficiency as a critical problem in wheat production in Central Anatolia. Plant Soil 180 (2), 165 172. Cary, E.E., 1982. Chromium in air, soil and natural waters. Biol. Environ. Aspects Chromium 5, 49 64. Chaffai, R., Koyama, H., 2011. Heavy metal tolerance in Arabidopsis thaliana, Advances in Botanical Research, vol. 60. Academic Press, pp. 1 49.

Plant Life under Changing Environment

References

283

Chaney, R.L., 1988. Metal speciation and interaction among elements affect trace element transfer in agricultural and environmental food-chains. Metal Precipitation: Theory, Analysis, and Application. Lewis Publications, pp. 219 259. Chaney, R.L., Brown, J.C., Tiffin, L.O., 1972. Obligatory reduction of ferric chelates in iron uptake by soybeans. Plant Physiol. 50 (2), 208 213. Chmielewska, E., Spiegel, H., 2003. Some control of an amplified heavy metal distribution at immission sites of Danube lowland refineries. Environ. Protect. Eng. 29 (2), 23 32. Choppala, G., Saifullah, Bolan, N., Bibi, S., Iqbal, M., Rengel, Z., et al., 2014. Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit. Rev. Plant Sci. 33 (5), 374 391. Clemens, S., 2001. Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212 (4), 475 486. Cobbett, C.S., 2000. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 123 (3), 825 832. Cobbett, C., Goldsbrough, P., 2002. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 53 (1), 159 182. Costa, G., Morel, J.L., 1994. Water relations, gas exchange and amino acid content in Cd-treated lettuce. Plant Physiol. Biochem. (France) 32, 561 570. Dalvi, A.A., Bhalerao, S.A., 2013. Response of plants towards heavy metal toxicity: an overview of avoidance, tolerance and uptake mechanism. Ann. Plant Sci. 2 (09), 362 368. de Freitas-Silva, L., de Arau´jo, T.O., da Silva, L.C., de Oliveira, J.A., de Araujo, J.M., 2016. Arsenic accumulation in Brassicaceae seedlings and its effects on growth and plant anatomy. Ecotoxicol. Environ. Saf. 124, 1 9. Delmail, D., Labrousse, P., Hourdin, P., Larcher, L., Moesch, C., Botineau, M., 2011. Differential responses of Myriophyllum alterniflorum DC (Haloragaceae) organs to copper: physiological and developmental approaches. Hydrobiologia 664 (1), 95 105. Deng, D., Wu, S.C., Wu, F.Y., Deng, H., Wong, M.H., 2010. Effects of root anatomy and Fe plaque on arsenic uptake by rice seedlings grown in solution culture. Environ. Pollut. 158 (8), 2589 2595. Ekmekc¸i, Y., Tanyolac¸, D., Ayhan, B., 2009. A crop tolerating oxidative stress induced by excess lead: maize. Acta Physiol. Plant. 31 (2), 319 330. Fageria, N.K., Filho, M.B., Moreira, A., Guimara˜es, C.M., 2009. Foliar fertilization of crop plants. J. Plant Nutr. 32 (6), 1044 1064. Flora, S.J., 2011. Arsenic-induced oxidative stress and its reversibility. Free Radical Biol. Med. 51 (2), 257 281. Foy, C.D., Chaney, R.T., White, M.C., 1978. The physiology of metal toxicity in plants. Annu. Rev. Plant Physiol. 29 (1), 511 566. Gabrielli, R., Sanita` di Toppi, L., 1999. Response to cadmium in higher plants. Environ. Exp. Bot. 41, 105 130. Garg, N., Singla, P., 2011. Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environ. Chem. Lett. 9 (3), 303 321. Goix, S., Mombo, S., Schreck, E., Pierart, A., Le´veˆque, T., Deola, F., et al., 2015. Field isotopic study of lead fate and compartmentalization in earthworm soil metal particle systems for highly polluted soil near Pb recycling factory. Chemosphere 138, 10 17. Goldsbrough, P., 2000. 12: Metal tolerance in plants: the role of phytochelatins and metallothioneins. In: Phytoremediation of Contaminated Soil and Water. CRC Press, p. 221. Guerinot, M.L., 2000. The ZIP family of metal transporters. Biochim. Biophys. Acta (BBA)—Biomembranes 1465 (1 2), 190 198. Gupta, S., Chakrabarti, S.K., 2013. Effect of heavy metals on different anatomical structures of Bruguiera sexangula. Int. J. Bio-Resour. Stress Manage. 4 (4), 605 609. Hall, J.L., 2002. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53 (366), 1 11. Han, F.X., Sridhar, B.M., Monts, D.L., Su, Y., 2004. Phytoavailability and toxicity of trivalent and hexavalent chromium to Brassica juncea. New Phytol. 162 (2), 489 499. Harguinteguy, C.A., Cofre´, M.N., Ferna´ndez-Cirelli, A., Pignata, M.L., 2016. The macrophytes Potamogeton pusillus L. and Myriophyllum aquaticum (Vell.) Verdc. as potential bioindicators of a river contaminated by heavy metals. Microchem. J. 124, 228 234. Hernandez, L.E., Carpena-Ruiz, R., Garate, A., 1996. Alterations in the mineral nutrition of pea seedlings exposed to cadmium. J. Plant Nutr. 19 (12), 1581 1598. Horst, W.J., Marschner, H., 1978. ). Effect of silicon on manganese tolerance of bean plants (Phaseolus vulgaris L.). Plant Soil 50 (1 3), 287 303.

Plant Life under Changing Environment

284

12. Heavy metal stress and plant life: uptake mechanisms, toxicity, and alleviation

Hossain, M.A., Piyatida, P., da Silva, J.A.T., Fujita, M., 2012. Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. 2012, 1 37. Available from: https://doi.org/10.1155/2012/872875. Hussain, D., Haydon, M.J., Wang, Y., Wong, E., Sherson, S.M., Young, J., et al., 2004. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16 (5), 1327 1339. Iwasaki, K.Z., Sakurai, K., Takahashi, E., 1990. Copper binding by the root cell walls of Italian ryegrass and red clover. Soil Sci. Plant Nutr. 36 (3), 431 439. Ja¨rup, L., 2003. Hazards of heavy metal contamination. Br. Med. Bull. 68 (1), 167 182. Jonak, C., Nakagami, H., Hirt, H., 2004. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol. 136 (2), 3276 3283. Kabata-Pendias, A., Mukherjee, A.B., 2007. Trace Elements From Soil to Human. Springer Science & Business Media. Kabata-Pendias, A., Pendias, H., 1984. Trace Elements in Soil and Plants (No. 631.41 K3). Kafka, Z., Puncocharova, J., 2002. Toxicity of heavy metals in nature. Chemicke´listy 96 (7), 611 617. Kanazawa, K., Higuchi, K., Nishizawa, N.K., Fushiya, S., Chino, M., Mori, S., 1994. Nicotianamine aminotransferase activities are correlated to the phytosiderophore secretions under Fe-deficient conditions in Gramineae. J. Exp. Bot. 45 (12), 1903 1906. Klapheck, S., Schlunz, S., Bergmann, L., 1995. Synthesis of phytochelatins and homo-phytochelatins in Pisum sativum L. Plant Physiol. 107 (2), 515 521. Kra¨mer, U., Cotter-Howells, J.D., Charnock, J.M., Baker, A.J., Smith, J.A.C., 1996. Free histidine as a metal chelator in plants that accumulate nickel. Nature 379 (6566), 635 638. Lasat, M.M., 2002. Phytoextraction of toxic metals. J. Environ. Qual. 31 (1), 109 120. Li, Z., Ma, Z., van der Kuijp, T.J., Yuan, Z., Huang, L., 2014. A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci. Total Environ. 468, 843 853. Lux, A., Vaculı´k, M., Martinka, M., Liˇskova´, D., Kulkarni, M.G., Stirk, W.A., et al., 2010. Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medicinal plant Merwilla plumbea. Ann. Bot. 107 (2), 285 292. Masion, A., Bertsch, P.M., 1997. Aluminium speciation in the presence of wheat root cell walls: a wet chemical study. Plant Cell Environ. 20 (4), 504 512. Meharg, A.A., Macnair, M.R., 1990. An altered phosphate uptake system in arsenate-tolerant Holcus lanatus L. New Phytol. 116 (1), 29 35. Niazi, N.K., Burton, E.D., 2016. Arsenic sorption to nanoparticulate mackinawite (FeS): an examination of phosphate competition. Environ. Pollut. 218, 111 117. Norgate, T.E., Jahanshahi, S., Rankin, W.J., 2007. Assessing the environmental impact of metal production processes. J. Cleaner Prod. 15 (8 9), 838 848. Norouzi, S., Khademi, H., Cano, A.F., Acosta, J.A., 2016. Biomagnetic monitoring of heavy metals contamination in deposited atmospheric dust, a case study from Isfahan, Iran. J. Environ. Manage. 173, 55 64. Nriagu, J.O., 1979. Copper in the Environment: Part I: Ecological Cycling. Wiley-Interscience. Panou-Filotheou, H., Bosabalidis, A.M., 2004. Root structural aspects associated with copper toxicity in oregano (Origanum vulgare subsp. hirtum). Plant Sci. 166 (6), 1497 1504. Peleg, Z., Blumwald, E., 2011. Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 14 (3), 290 295. Peterson, P.J., Alloway, B.J., 1979. Cadmium in soils and vegetation. Topics Environ. Health. Pickering, 2, 4592. Pickering, I.J., Prince, R.C., George, M.J., Smith, R.D., George, G.N., Salt, D.E., 2000. Reduction and coordination of arsenic in Indian mustard. Plant Physiol. 122 (4), 1171 1178. Pilon-Smits, E., 2005. Phytoremediation. Annu. Rev. Plant Biol. 56, 15 39. Pilon-Smits, E., Pilon, M., 2002. Phytoremediation of metals using transgenic plants. Crit. Rev. Plant Sci. 21 (5), 439 456. Popova, L.P., Maslenkova, L.T., Yordanova, R.Y., Ivanova, A.P., Krantev, A.P., Szalai, G., et al., 2009. Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol. Biochem. 47 (3), 224 231.

Plant Life under Changing Environment

References

285

Poschenrieder, C., Gunse, B., Barcelo, J., 1989. Influence of cadmium on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. Plant Physiol. 90 (4), 1365 1371. Pourrut, B., Shahid, M., Douay, F., Dumat, C., Pinelli, E., 2013. Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. Heavy Metal Stress in Plants. Springer, Berlin, Heidelberg, pp. 121 147. Rascio, N., Navari-Izzo, F., 2011. Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci. 180 (2), 169 181. Reichman, S.M., 2002. The Responses of Plants to Metal Toxicity: A Review Forusing on Copper, Manganese & Zinc. Australian Minerals & Energy Environment Foundation, Melbourne, pp. 22 26. Robinson, N.J., Tommey, A.M., Kuske, C., Jackson, P.J., 1993. Plant metallothioneins. Biochem. J. 295 (Pt 1), 1. Ro¨mheld, V., Marschner, H., 1986. Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol. 80 (1), 175 180. Saher, N.U., Siddiqui, A.S., 2016. Comparison of heavy metal contamination during the last decade along the coastal sediment of Pakistan: multiple pollution indices approach. Mar. Pollut. Bull. 105 (1), 403 410. Salomons, W., Fo¨rstner, U., 2012. Metals in the Hydrocycle. Springer Science & Business Media. Salt, D.E., Prince, R.C., Pickering, I.J., Raskin, I., 1995. Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol. 109 (4), 1427 1433. Sarma, H., 2011. Metal hyperaccumulation in plants: a review focusing on phytoremediation technology. J. Environ. Sci. Technol. 4 (2), 118 138. Sarwar, N., Malhi, S.S., Zia, M.H., Naeem, A., Bibi, S., Farid, G., 2010. Role of mineral nutrition in minimizing cadmium accumulation by plants. J. Sci. Food Agric. 90 (6), 925 937. Schat, H., Llugany, M., Vooijs, R., Hartley-Whitaker, J., Bleeker, P.M., 2002. The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J. Exp. Bot. 53 (379), 2381 2392. Senden, M.H.M.N., Wolterbeek, H.T., 1990. Effect of citric acid on the transport of cadmium through xylem vessels of excised tomato stem-leaf systems. Acta Bot. Neerl. 39 (3), 297 303. Seth, C.S., 2012. A review on mechanisms of plant tolerance and role of transgenic plants in environmental cleanup. Bot. Rev. 78 (1), 32 62. Seth, C.S., Chaturvedi, P.K., Misra, V., 2007. Toxic effect of arsenate and cadmium alone and in combination on giant duckweed (Spirodela polyrrhiza L.) in response to its accumulation. Environ. Toxicol. 22 (6), 539 549. Shahid, M., Pourrut, B., Dumat, C., Nadeem, M., Aslam, M., Pinelli, E., 2014. Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants, Reviews of Environmental Contamination and Toxicology, vol. 232. Springer, Cham, pp. 1 44. Shahid, M., Khalid, S., Abbas, G., Shahid, N., Nadeem, M., Sabir, M., et al., 2015. Heavy metal stress and crop productivity. Crop Production and Global Environmental Issues. Springer, Cham, pp. 1 25. Shahid, M., Shamshad, S., Rafiq, M., Khalid, S., Bibi, I., Niazi, N.K., et al., 2017. Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178, 513 533. Shanker, A.K., Cervantes, C., Loza-Tavera, H., Avudainayagam, S., 2005. Chromium toxicity in plants. Environ. Int. 31 (5), 739 753. Sharma, S.S., Dietz, K.J., 2009. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 14, 43 50. Sharma, D.C., Sharma, C.P., Tripathi, R.D., 2003. Phytotoxic lesions of chromium in maize. Chemosphere 51 (1), 63 68. Sheoran, I.S., Singh, R., 1993. Effect of heavy metals on photosynthesis in higher plants. Photosynthesis: Photoreactions to Plant Productivity. Springer, Dordrecht, pp. 451 468. Shi, G.R., Cai, Q.S., 2008. Photosynthetic and anatomic responses of peanut leaves to cadmium stress. Photosynthetica 46 (4), 627 630. Siciliano, S.D., Germida, J.J., 1998. Mechanisms of phytoremediation: biochemical and ecological interactions between plants and bacteria. Environ. Rev. 6 (1), 65 79. Singh, H.P., Batish, D.R., Kohli, R.K., Arora, K., 2007. Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb.) is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul. 53 (1), 65 73. Singh, D., Chauhan, S.K., 2011. Organic acids of crop plants in alumium detoxification. Curr. Sci. 100, 1509 1515.

Plant Life under Changing Environment

286

12. Heavy metal stress and plant life: uptake mechanisms, toxicity, and alleviation

Siqueira-Silva, A.I., da Silva, L.C., Azevedo, A.A., Oliva, M.A., 2012. Iron plaque formation and morphoanatomy of roots from species of restinga subjected to excess iron. Ecotoxicol. Environ. Saf. 78, 265 275. Sridhar, K.R., Ba¨rlocher, F., Krauss, G.J., Krauss, G., 2005. Response of aquatic hyphomycete communities to changes in heavy metal exposure. Int. Rev. Hydrobiol. 90 (1), 21 32. Stoeva, N., Bineva, T., 2003. Oxidative changes and photosynthesis in oat plants grown in As-contaminated soil. Bulg. J. Plant Physiol. 29 (1 2), 87 95. Sunitha, M.S., Prashant, S., Kumar, S.A., Rao, S.R.I.N.A.T.H., Narasu, M.L., Kishor, P.K., 2013. Cellular and molecular mechanisms of heavy metal tolerance in plants: a brief overview of transgenic plants overexpressing phytochelatin synthase and metallothionein genes. Plant Cell Biotechnol. Mol. Biol. 14 (1 2), 33 48. ´ Szyczewski, P., Siepak, J., Niedzielski, P., Sobczynski, T., 2009. Research on heavy metals in Poland. Pol. J. Environ. Stud. 18 (5), 755. Taiz, L., Zeiger, E., 2002. Plant Physiology. Sinauer Associates. Talukdar, D., 2013. Arsenic-induced oxidative stress in the common bean legume, Phaseolus vulgaris L. seedlings and its amelioration by exogenous nitric oxide. Physiol. Mol. Biol. Plants 19 (1), 69 79. Tanhan, P., Kruatrachue, M., Pokethitiyook, P., Chaiyarat, R., 2007. Uptake and accumulation of cadmium, lead and zinc by Siam weed [Chromolaena odorata (L.) King & Robinson]. Chemosphere 68 (2), 323 329. Thomine, S., Wang, R., Ward, J.M., Crawford, N.M., Schroeder, J.I., 2000. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. 97 (9), 4991 4996. Tong, Y.P., Kneer, R., Zhu, Y.G., 2004. Vacuolar compartmentalization: a second-generation approach to engineering plants for phytoremediation. Trends Plant Sci. 9 (1), 7 9. Torres, M.A., Barros, M.P., Campos, S.C., Pinto, E., Rajamani, S., Sayre, R.T., et al., 2008. Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol. Environ. Saf. 71 (1), 1 15. Tripathi, R.D., Srivastava, S., Mishra, S., Singh, N., Tuli, R., Gupta, D.K., et al., 2007. Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotechnol. 25 (4), 158 165. Tripathi, D.K., Singh, V.P., Kumar, D., Chauhan, D.K., 2012. Impact of exogenous silicon addition on chromium uptake, growth, mineral elements, oxidative stress, antioxidant capacity, and leaf and root structures in rice seedlings exposed to hexavalent chromium. Acta Physiol. Plant. 34 (1), 279 289. Vatamaniuk, O.K., Mari, S., Lang, A., Chalasani, S., Demkiv, L.O., Rea, P.A., 2004. Phytochelatin synthase, a dipeptidyl transferase that undergoes multisite acylation with γ-glutamylcysteine during catalysis. Stoichiometric and site-directed mutagenic analysis of AtPCS1-catalyzed phytochelatin synthesis. J. Biol. Chem. 279, 22449 22460. Available from: https://doi.org/10.1074/jbc.M313142200. Volkering, F., Breure, A.M., Rulkens, W.H., 1997. Microbiological aspects of surfactant use for biological soil remediation. Biodegradation 8 (6), 401 417. Walton, J.D., 1994. Deconstructing the cell wall. Plant Physiol. 104 (4), 1113. Williams, L.E., Pittman, J.K., Hall, J.L., 2000. Emerging mechanisms for heavy metal transport in plants. Biochim. Biophys. Acta (BBA)-Biomembranes 1465 (1 2), 104 126. Wu, L.H., Luo, Y.M., Xing, X.R., Christie, P., 2004. EDTA-enhanced phytoremediation of heavy metal contaminated soil with Indian mustard and associated potential leaching risk. Agric. Ecosyst. Environ. 102 (3), 307 318. Yang, X.E., Jin, X.F., Feng, Y., Islam, E., 2005. Molecular mechanisms and genetic basis of heavy metal tolerance/ hyperaccumulation in plants. J. Integr. Plant Biol. 47, 1025 1035. Zeid, I.M., 2001. Responses of Phaseolus vulgaris chromium and cobalt treatments. Biol. Plant. 44 (1), 111 115. Zhang, Q., Yan, C., Liu, J., Lu, H., Wang, W., Du, J., et al., 2013. Silicon alleviates cadmium toxicity in Avicennia marina (Forsk.) Vierh. seedlings in relation to root anatomy and radial oxygen loss. Mar. Pollut. Bull. 76 (1 2), 187 193.

Further reading Atsdr, U., 2007. Toxicological Profile for Arsenic. Agency for Toxic Substances and Disease Registry, Division of Toxicology, Atlanta, GA. Carbonell-Barrachina, A.A., Burlo´, F., Mataix, J., 1998. Response of bean micronutrient nutrition to arsenic and salinity. J. Plant Nutr. 21 (6), 1287 1299.

Plant Life under Changing Environment

Further reading

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Ho, B., Edith, L., 2002. Conceptosba´sicos de la contaminacio´n del agua y para´metros de medicio´n. CursoInternacionalGestio´n Integral del Tratamiento de AguasResiduales. UNC, pp. 1 51. Jiang, Q.Q., Singh, B.R., 1994. Effect of different forms and sources of arsenic on crop yield and arsenic concentration. Water Air Soil Pollut. 74 (3 4), 321 343. Mokgalaka-Matlala, N.S., Flores-Tavizo´n, E., Castillo-Michel, H., Peralta-Videa, J.R., Gardea-Torresdey, J.L., 2008. Toxicity of arsenic (III) and (V) on plant growth, element uptake, and total amylolytic activity of mesquite (Prosopis juliflora 3 P. velutina). Int. J. Phytorem. 10 (1), 47 60. Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8 (3), 199 216. Shaibur, M.R., Kitajima, N., Sugawara, R., Kondo, T., Alam, S., Huq, S.I., et al., 2008. Critical toxicity level of arsenic and elemental composition of arsenic-induced chlorosis in hydroponic sorghum. Water Air Soil Pollut. 191 (1 4), 279 292. Srivastava, S., Srivastava, A.K., Suprasanna, P., D’souza, S.F., 2009. Comparative biochemical and transcriptional profiling of two contrasting varieties of Brassica juncea L. in response to arsenic exposure reveals mechanisms of stress perception and tolerance. J. Exp. Bot. 60 (12), 3419 3431. Tu, C., Ma, L.Q., 2002. Effects of arsenic concentrations and forms on arsenic uptake by the hyperaccumulator ladder brake. J. Environ. Qual. 31 (2), 641 647.

Plant Life under Changing Environment

C H A P T E R

13 Nanoparticles in plants: morphophysiological, biochemical, and molecular responses Fabia´n Pe´rez-Labrada1, Hipo´lito Herna´ndez-Herna´ndez2, Mari Carmen Lo´pez-Pe´rez1, Susana Gonza´lez-Morales3, Adalberto Benavides-Mendoza1 and Antonio Jua´rez-Maldonado4 1

Department of Horticulture, Autonomous Agrarian University Antonio Narro, Saltillo, Mexico 2Papaloapan University, Loma Bonita, Oaxaca, Mexico 3CONACyT-Department of Horticulture, Autonomous Agrarian University Antonio Narro, Saltillo, Mexico 4 Department of Botany, Autonomous Agrarian University Antonio Narro, Saltillo, Mexico

13.1 Introduction Different environmental factors, by inducing stress conditions in plants, represent great challenges in crop production (Adger et al., 2009). These conditions limit productivity when plants make biochemical, physiological, or genetic adjustments (Vishwakarma et al., 2017; Kosova´ et al., 2018), which translate into an extra cost of energy. Production of greenhouse crops is an alternative for adverse environmental conditions management, reducing negative effects and even increasing productivity (Clark and Tilman, 2017). However, problems, such as soil salinity, high or low temperatures, deficit of nutrients, and heavy metals, have a major impact on productivity. Nanotechnology is a science that has great importance in agriculture, due to the potential benefits it represents (Servin and White, 2016). Many researches on the effect of nanoparticles (NPs) (,100 nm) on crops have been conducted (Rajput et al., 2017). However, most of the research carried out has focused on assessing the risks posed by NPs to plants (Du et al., 2017; Tripathi et al., 2017b; Rajput et al., 2017).

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00016-3

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Currently, there are studies about the use of NPs that show the beneficial effects in different crops. Several effects have been reported, such as the increase in Solanum lycopersicum L. (Shankramma et al., 2016) and Allium cepa L. (Anandaraj and Natarajan, 2017) germination; greater growth in S. lycopersicum L. plants (Jua´rez-Maldonado et al., 2016; Herna´ndez-Herna´ndez et al., 2017), strawberry (Mozafari et al., 2018), rice (Mankad et al., 2017; Singh et al., 2018); quality increase in tomato fruit (Jua´rez-Maldonado et al., 2016; Herna´ndez-Herna´ndez et al., 2017; Herna´ndez-Fuentes et al., 2017), jalapen˜o pepper (Pinedo-Guerrero et al., 2017), strawberry (Mozafari et al., 2018); and even increasing the ´ vase life of different ornamental plants (Amingad et al., 2017; Byczynska, 2017; Mohammadbagheri and Naderi, 2017; Park et al., 2017). In addition, beneficial effects on the application of different NPs in cultures developed under conditions of abiotic stress have been demonstrated. Studies have been carried out under saline stress conditions (Askary et al., 2017; Rossi et al., 2017; Herna´ndezHerna´ndez et al., 2018), drought stress (Mozafari et al., 2018), stress due to high temperatures (Asadapour et al., 2016) or low temperatures (Mohammadi et al., 2014; Hasanpour et al., 2015), heavy metal stress (Gowayed and Kadasa, 2016; Tripathi et al., 2016), and even nutrient deficit (Zahra et al., 2015; Raliya et al., 2016). The potential positive effects of NPs are related to physiological, biochemical, genetic, and morphological changes (Monica and Cremonini, 2009; Tripathi et al., 2017b). Therefore a greater tolerance to various conditions of abiotic stress has been observed. With this in mind, it is possible to use NPs in crops as a new tool against the different negative effects caused by abiotic stress. This chapter describes the use of NPs in plants as a practical tool to minimize the harmful effects caused by different types of abiotic stress. The different effects induced by the application of NPs on the morphological and biochemical characteristics are explained, as well as the transcriptomic and proteomic responses of the plants, and their relationship with stress tolerance. In addition, the most recent information on the use of NPs and its positive effects that induce tolerance to various conditions of abiotic stress in crops will be shown.

13.2 Nanotechnology and nanoparticles Nanotechnology is commonly defined as the study, application, and manipulation of matter at an atomic, molecular, and supramolecular scale. In recent years, nanotechnology applications have grown surprisingly in several sectors. So much so that the European Commission classifies it as a “key enabling technology” that favors sustainable competitiveness (Gallocchio et al., 2015; Parisi et al., 2015). This has allowed the development and manipulation of structures and devices (1
100 nm in at least one dimension) called nanomaterials, characteristics of which provide new complex functions (Salata, 2004; McNeil, 2005; Qu et al., 2013). These nanomaterials have supported interdisciplinary research. Their use has spread in different areas such as medicine to diagnose and treat diseases such as cancer (Cheng et al., 2015; Mohammed et al., 2017; Hong and Dobrovolskaia, 2018; Huang et al., 2018), or microbiology (Le Ouay and Stellacci, 2015; Alves et al., 2018), in molecular biology (Jasinski et al., 2017; Nummelin et al., 2018), oil and gas industry (Fakoya and Shah, 2017),

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for water and wastewater treatment (Qu et al., 2013) or to mitigate environmental pollution (Yunus et al., 2012). Agriculture is another field of nanomaterial application (Baruah and Dutta, 2009), where nanoformulation of agrochemicals (fertilizers, pesticides, and herbicides) has been used to control their release, or specific supply of biomolecules, nanosensors and nanoarrays of diseases and agrochemicals residues, nanodevices for genetic manipulation, diagnosis of plant diseases, health, and postharvest management and food processing (Chellaram et al., 2014; Sekhon, 2014; Kumari and Yadav, 2014; Gallocchio et al., 2015; Wang et al., 2016a; Kim et al., 2018). Nanomaterials include NPs (Salata, 2004; Biswas and Wu, 2005) characteristics (shape, high surface area, load, chemical properties, solubility, and degree of agglomeration) and multifunctionality of which have allowed them to be used in various areas of engineering, cosmetics, medicine, and agriculture (McNeil, 2005; Fakoya and Shah, 2017; Alves et al., 2018; Hong and Dobrovolskaia, 2018; Naderi et al., 2018). Particularly in the agriculture, NPs have been studied as sources of fertilizers that increase crop yields, mitigate environmental pressures, and increase the nutraceutical quality of plants and fruits, thus generating functional foods (Arruda et al., 2015; Liu and Lal, 2015; Mishra et al., 2017; Duhan et al., 2017; Thiruvengadam et al., 2018). Although there is a great diversity of NPs, they obtained from essential metals (Zn, Fe, Mn, Cu among others), and their oxides have proven to be more suitable to use in agriculture (Ruttkay-Nedecky et al., 2017).

13.3 Impacts of nanoparticles in plants The positive effect of NPs depends on their own characteristics, such as shape, surface properties (Singh et al., 2018), size (Hou et al., 2018), exposure time (Yanık and Vardar, 2015), and concentration used (Rizwan et al., 2017). Some other significant factors are crop management, plant species (Jo´sko et al., 2017), age, soil type, substrate, or hydroponic environment, among others (Tripathi et al., 2017b). NPs have different effects on plants, and they even generate different responses depending on the type of stress they interact with. There is a wide range of effects derived from physiological, biochemical, genetic, and morphological changes, as well as changes in plant anatomy and histology (Monica and Cremonini, 2009; Tripathi et al., 2017b).

13.3.1 Morphological, anatomical, and histological changes induced by nanoparticles Plant anatomical structures are an important characteristic; however, little has been studied on how plants are affected with the application of NPs. The determination of the anatomical characteristics in the plants will help to have a broader focus on the modifications and adaptation strategies that are followed under an adverse environmental condition (Tripathi et al., 2016). Therefore it is important to consider this type of characteristics when working with NPs and stress. The application of different NPs to plants has potential beneficial effects due to morphological, anatomical, and histological modifications, which are explained later (Fig. 13.1).

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FIGURE 13.1

13. Nanoparticles in plants: morphophysiological, biochemical, and molecular responses

Morphological, anatomical, and histological responses of nanoparticles on plants against

abiotic stresses.

The modification of stomata is of great interest for researchers, since there is an exchange of gases between plants and their environment throughout these structures, which directly influences their ability to carry out photosynthesis (Dittberner et al., 2018). Gonza´lez-Go´mez et al. (2017) reported an increase in stoma width in Citrullus lanatus L. by applying chitosan
polyvinyl alcohol hydrogels (Cs
PVA) hydrogels with Cu NPs. Da Costa and Sharma (2016) found smaller stomata and in smaller number, as well as an increase of trichomes in leaves of Oryza sativa L. when applying CuO NPs. The same authors concluded that the morphological modifications of roots reduced water uptake which in turn influenced the modification of stomata. In addition, CuO NPs can induce an increase in H2O2 due to oxidative stress, increase the level of Ca in the guard cells, which finally manifests in the closure of stomata (Zhao et al., 2017a). Likewise, the morphological variations observed in stomata can also be derived from biochemical and physiological changes, and from the activation of response genes (Zhao et al., 2017b).

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Corredor et al. (2009) concluded that Cucurbita pepo L. cells could respond to the presence of Fe NP aggregates by changing their subcellular organization. In Lolium perenne L. the application of ZnO NPs at 1000 mg/L causes irregularities in the morphology of root tips (cortex and epidermis) (Lin and Xing, 2008; Ma et al., 2010). Likewise, the accumulation of TiO2 NPs on the cell wall surfaces of the primary root of Zea mays L. led to different changes at the morphological level, in the epidermal cell wall the pore size was inhibited, the water transport decreased, which also affects the transpiration rate, and the growth of the leaf decreased (Asli and Neumann, 2009). Pokhrel and Dubey (2013) observed that Ag and ZnO NPs in Z. mays L. lengthened the primary root cells in the elongation zone, possibly by the induction of gibberellins mediated by NPs. Tripathi et al. (2017a) mentioned that the application of Ag NPs on Cucumis sativus L. causes modifications in the wall of cortical cells, growth of lateral and secondary roots, as well as changes in cell division due to an improvement in the xylem and secondary phloem. Plants develop apoplastic barriers in their root to defend themselves from the stress caused by toxic ions (Vaculı´k et al., 2012; Rossi et al., 2015), so it is possible that NPs can positively influence this stress. Rossi et al. (2017) reported that CeO2 NPs produced anatomical changes at the root apex of Brassica napus L. by decreasing apoplastic barriers, these changes raised the capacity of the plant to develop under saline stress conditions. Yanık and Vardar (2015) found that an application of 50 mg/L of Al2O3 NPs (13 nm) caused phytotoxicity in Triticum aestivum L., generating accumulation of lignin, callose deposition, and damage to cortex cells of the root parenchyma, reducing its elongation. It has been reported that stress due to CuO NPs causes accumulation of lignin in the roots of S. lycopersicum L. and Brassica oleracea L. (Singh et al., 2017), as well as in roots of Arabidopsis thaliana L. (Nair and Chung, 2014), this is possible because the CuO NPs can move through the plant’s conductive tissues (xylem and phloem), which allows them to go from the roots to the shoots or vice versa (Li et al., 2017; Ma et al., 2017). Therefore the NPs can interact with different compounds such as organic acids and proteins (Shi et al., 2014), this can result in the dissolution of CuO NPs that can be transformed to its ionic form ðCu21 Þ, which ultimately stimulates the accumulation of lignin (Nair and Chung, 2014; Singh et al., 2017). The lignin generates resistance and hardness of plant tissues by means of links with the elements of the cell wall, and in some cases the lignin can hinder the movement of toxic elements in the Casparian strip of the endodermis and exodermis wall (Cai et al., 2017; Byrt et al., 2018). Foliar application of Si NPs (5
15 nm) in Jatropha integerrima under salt stress increased mesophyll, palisade, and spongy parenchyma thickness (Ashour and Mahmoud, 2017). Si NPs (10
100 nm) can accumulate over the entire surface or be aligned within the leaf blade, providing structural support and flexibility to the leaves (Sato et al., 2017). The accumulation and availability of Si NPs in T. aestivum L. reduces stress due to UV-B radiation, since it improves the lignification and suberization of bundle sheath cells and metaxylem vessels, protecting the degradation of palisade and mesophilic cells (Tripathi et al., 2017c). In addition, it has been observed that Si NPs can be related to tolerance to stress caused by salinity, by affecting xylem moisture and hydraulic conductivity in Ocimum basilicum L. (Kalteh et al., 2014). CuO NPs induced morphological changes in Hordeum vulgare L., causing a decrease in the stem and root length (Rajput et al., 2017). In O. sativa L., a decrease in shoot values

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and root length was showed due to the accumulation of Cu in roots and foliar tissue with the same type of NPs (Da Costa and Sharma, 2016). Nair and Chung (2015) found that the application of Ag NPs reduced the shoot length and weight when a concentration of 50 mg/L was used, and root length and weight with both 20 and 50 mg/L concentrations in Vigna radiata L. The application at 7.5 ppm of Ag NPs increased plant height, leaf length, and width of Chrysanthemum morifolium L. (Tung et al., 2018). The application of Ag1 NPs generated a greater flower diameter in Paeonia lactiflora Pall (Zhao et al., 2018). Exposure of T. aestivum L., during 60 days at 60 mg/kg of TiO2 NPs (,20 nm), induced an increase in root and shoot length; however, higher concentrations caused toxicity (Rafique et al., 2018). Under Zn deficiency, the application of ZnO NPs caused greater stem and root length in Arachis hypogaea L. (Rajiv and Vanathi, 2018). In Phaseolus vulgaris L. an increase of root and leaf length was showed when use 500 mg/kg of coated ZnO NPs (Medina-Velo et al., 2017). Yang et al. (2017) reported a positive effect of NPs (CuO and ZnO) under drought stress when root hairs and lateral roots of T. aestivum L. increased. Soltani et al. (2017) reported that the use of silicon NPs (1000 ppm) in Solanum tuberosum L. improved leaf area, stem height, cumulative length, and root surface area, increasing the root efficiency during water and nutrients uptake, mitigating the effects of drought stress and nutrient deficit. In Glycine max L., SiO2 NPs (0.5 and 1 mM) improved shoot and root growth (Farhangi-Abriz and Torabian, 2018). Under adverse environmental conditions, the plants present morphological, anatomical, and histological changes, these alterations can be reduced with the application of NPs or induce beneficial changes in these levels by modifying the leaf organization, increasing the chloroplasts number, greater grana stacking and vascular bundles (Yuan et al., 2018), and increasing stoma width (Gonza´lez-Go´mez et al., 2017) and trichomes (Da Costa and Sharma, 2016). Similarly, they can induce greater thickness of the leaf, palisade and spongy parenchyma (Ashour and Mahmoud, 2017) and greater lignification and suberization of bundle sheath cells and metaxylem vessels of the leaves (Tripathi et al., 2017c) and root (Singh et al., 2017). They also modify the cortical cells increasing the growth of lateral and secondary roots (Tripathi et al., 2017a). These changes induced by the NPs (particularly Fe, Cu, Si, and Ag NPs) can improve the tolerance or mitigate the abiotic stress to which the plant is subjected.

13.3.2 Induction of antioxidant compounds by nanoparticles 13.3.2.1 Oxidative stress Plants are subject to stressing environments that can cause alterations in energy balance (production/consumption), which is regulated by means of a series of metabolic processes related to the transfer of electrons, substrates, and reducers. These processes of gradient reduction carried out in different cellular compartments allow the generation of different reactive species that can be oxygen (ROS), or nitrogen (RNS) to a lesser extent, which remains at moderate levels. This ROS function as signal transducers (Suzuki et al., 2012). Nonradical species, such as dioxygen (3O2), singlet oxygen (1O2), peroxide ðO22 2 Þ, hydrogen 2 22 peroxide (H2O2), oxene ion (O ), oxide ion (O ), and superoxide-free radicals ðO2 2 Þ,
•  perhydroxyl HO2 , and hydroxyl (OH ) are considered among the main components of

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ROS (Gill and Tuteja, 2010; Yin et al., 2010). The O2 2 , H2O2, and HO2 are originated by O2 electron reduction and by the processes of dismutation and protonation of the same compounds (Gill and Tuteja, 2010). The same
authors point out that transition metals such as Cu and Fe can generate ROS, such as HO2 , from the Fenton reactions. O2 can react with other free radicals. In 1O2 (generated by the photoexcitation of chlorophyll and its subsequent reaction with O2), an electron changes to a higher energy orbital, which results in the release of O2 from its restricted state of rotation (Gill and Tuteja, 2010). The highest production of nonradical species as 1O2 and O2 2 is carried out in the chloroplasts, specifically in photosystems I and II. In mitochondria the main sources of O2 are components of the electron chain, such as complex I and III, and ubiquinone. On the other hand, a greater generation of H2O2 is found in peroxisomes (Gill and Tuteja, 2010; Reddy et al., 2016). To maintain moderate levels of ROS, plants track and eliminate their concentrations through a network of redox enzymatic processes (redoxome). However, when there is an increase of ROS content (derived from some type of stress, abiotic for example) in the cellular compartments, oxidative stress occurs because the redoxome is unable to generate enough enzymes to dissipate ROS excess. This can generate different effects at a biochemical level such as lipid peroxidation or protein alteration, in addition it can generate genetic damage specifically in DNA (Yin et al., 2010; Suzuki et al., 2012). Lipid peroxidation results from the capture of electrons from cell membrane lipids by ROS, generating a decrease in physiological function and ultimately cell death (Reddy et al., 2016; ´ Szymanska et al., 2016). 13.3.2.2 Antioxidant capacity In plants, excess ROS causes damage that can be mitigated by a series of elements capable of dissipating oxidative stress such as the following enzymatic compounds which are ROS scavenging systems: superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), peroxidase (POD), glutathione (GSH) reductase (GR), monohydroascorbate reductase, dehydroascorbate reductase (DHAR), GSH POD (GPX), guaiacol POD, and GSH-S-transferase (GST) (Gill and Tuteja, 2010; Yanık and Vardar, 2015; Wang et al., 2016a; Khan et al., 2017). This set of enzymes is presented as the antioxidant defense system that controls the oxidation cascades, prevents oxidative damage by protecting plant cells from ROS. On the other hand, the most important nonenzymatic antioxidant compounds in plants that can dissipate ROS are GSH, vitamin A, vitamin C (ascorbic acid, ASH), vitamin E complex [α-tocopherol, tocotrienols, plastochromanol (PC) and its hydroxylated derivatives (PC
OH)], phenols, flavonoids, carotenoids, and anthocyanins ´ (Gill and Tuteja, 2010; Szymanska et al., 2016; Khan et al., 2017). There is a direct relationship between enzymatic and nonenzymatic components as some of them react with different active forms of oxygen keeping them at a low level (SOD, CAT, POD), and the other regenerates the oxidized antioxidants (GR and APX) (Gill and Tuteja, 2010). Enzymes with tetrameric heme CAT group can dismute H2O2 into H2O and O2. These enzymes have the highest rate of rotation, that is, they can dismute approximately 6 million molecules of H2O2 per minute and are presented as diverse isoenzymes (Gill and Tuteja, 2010; Wang et al., 2016a). On the other hand, the SOD enzyme in its different forms, such as Cu/Zn-SOD, Mn-SOD, and Fe-SOD, provides the first barrier that acts

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against ROS when dislodging O2 to H2O2 and its subsequent oxidation to O2. This 2 enzyme is located in different cellular compartments, and as an enzymatic antioxidant it is • the most efficient. The elimination of O2 2 decreases the risk of OH formation through the Haber
Weiss reaction that is catalyzed by a transition metal (Gill and Tuteja, 2010; Thuesombat et al., 2016). Another important enzyme is APX, as it participates in the detoxification of H2O2 in water
water through the ASH
GSH cycle, using ASH as an electron donor. This enzyme is shown in several isoforms, which, compared to CAT and POD, have a greater affinity for H2O2 (Gill and Tuteja, 2010). On the other hand, guaiacol peroxidase (GPOX) is an enzyme that works as a defense against biotic stresses by consuming H2O2. However, it differs from APX because it has other functions, for example, it breaks down indole-3-acetic acid (IAA) and also participates in the biosynthesis of lignin in cell walls (Gill and Tuteja, 2010). GR (flavoprotein oxidoreductase) belongs to the ASH
GSH cycle. Its fundamental role is to maintain a GSH-reduced state (by providing sulfhydryl groups and substrate for GST). It can catalyze the reduction of GSH disulfide (GSSG)-dependent NADPH to reduced GSH in the last step of the ASH
GSH cycle, thanks to its active thiol group (Gill and Tuteja, 2010; Thuesombat et al., 2016). GPX provides another mechanism to remove H2O2 by converting it into H2O through the oxide-reduction cycle of GS
ASH. GPX initially reduces the selenocysteine residue or active site cysteine to the intermediate selenium or sulfenic acid (
Se
OH or
S
OH) using GSH, which originates
Se
SG or thiol
S
SG, which in turn reacts with a second molecule of GSH to restore the active site selenocysteine or cysteine producing GSH in its oxidized form (GSSG). The cycle closes when GR reduces GSSG using NADPH (Labunskyy et al., 2014; Couto et al., 2016; Thuesombat et al., 2016). Regarding nonenzymatic antioxidants, ASH is considered the largest ROS scavenger • derived from its ability to donate electrons in the ASH
GSH cycle, where O2 2 and OH are eliminated, and α-tocopherol is regenerated (Gill and Tuteja, 2010). While GSH has the potential to scavenge most ROS, especially 1O2, H2O2, and OH•, it is also part of the antioxidant defense system due to the important role it plays. Regarding proline, it acts as osmoprotector, protein stabilizer, and metal chelator, inhibiting 1O2 and OH•. On the other hand, tocopherols stabilize the membranes and scavenge 1O2, the carotenoids play a photoprotective role by scavenging ROS (mainly 1O2). Flavonoids act as ROS scavengers locating and neutralizing radicals before damaging the cell (Gill and Tuteja, 2010; Mehrian et al., 2015). 13.3.2.3 Oxidative stress induced by nanoparticles Since NPs are extremely small (,100 nm), their foliar or soil application can induce a rapid and easy absorption and translocation (either by the root, lenticels or stomata, trichomes, and hydathodes) to the different cell compartments. This is possible because NPs can enter through the cell membrane in greater proportion during endocytosis or crossing through transport proteins or ion channels (Yin et al., 2010; Nair et al., 2010; Raliya et al., 2015; Hou et al., 2018). This results in rapid concentration and accumulation in the cytoplasm where they can interact with cellular organelles (Shobha et al., 2014). Since NPs can be transported through xylem and phloem depending on their type and size (Ma et al., 2017), some of them can accumulate (especially metallic NPs such as Cu, Ni, Zn, TiO2, and CeO2) either in the plasma membrane, apoplast, cytoplasm, chloroplasts,

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mitochondria, or peroxisomes. For this reason, they can lead to an excessive production of ROS from the Fenton reactions originated by the ability to alternate between their oxidation states (Gill and Tuteja, 2010; Boghossian et al., 2013; Khan et al., 2017; Hou et al., 2018), or by the reaction of the NPs with sulfhydryl and carboxyl groups, which causes alterations in the proteins and increases malonaldehyde (MDA) levels, a product of peroxidation (Mohsenzadeh and Moosavian, 2017; Marslin et al., 2017). These MDA levels activate antioxidant defense mechanisms that could remove excess ROS and reduce membrane damage (Wang et al., 2016a). In some cases, serving as a center for electron retransmission, NPs can decrease intracellular H2O2 concentrations and lipid peroxidation, by increasing the efficiency of redox reactions (Mallick et al., 2006). According to Hong et al. (2005a,b), Lei et al. (2007), and Pradhan et al. (2015), NPs can influence the photosynthetic process by improving energy absorption and transmission through alterations in electron transport. This can accelerate the photolysis of water and ´ therefore generate an excess of 1O2 inducing a stress state. Szymanska et al. (2016) mention that relationships between tocochromanol and plastoquinol (PQH2) may be linked to the production of 1O2 (under conditions of high irradiance) and probably under normal conditions. Therefore exposure to NPs can increase the production of 1O2 depending on alterations of the PC hydroxylate/PC ratio in leaves, thereby inducing oxidative stress. Singh et al. (2018) mention that the application of ZnO NPs in O. sativa L. increases the concentration of substances that react to thiobarbituric acid (TBARS, by-products of lipid peroxidation). They also increase radicals O2 2 and H2O2 but in a greater proportion in roots than in leaves. Thuesombat et al. (2016) mention that the contact of plant tissue with NPs increases the production of H2O2 and therefore an increase in APX activity. 13.3.2.4 Induction of antioxidant capacity by nanoparticles The increase of ROS within cellular compartments of plant tissue exposed to NPs triggers a signaling response (aided by cytosolic Ca21) through the induction of permeable Ca21 pores and the oxidation of apoplastic L-ascorbic acid (Sosan et al., 2016; Khan et al., 2017; Marslin et al., 2017; Hou et al., 2018). This results in an increase in the production of antioxidant compounds, both enzymatic and nonenzymatic, with the aim of reducing the effect of ROS (Thuesombat et al., 2016; Hou et al., 2018). Khan et al. (2017) found that NPs increase the ROS level which in turn activates the antioxidant defense system more efficiently, derived from the amplification of the stress signal. This is because NPs produce an effect similar to signaling molecules in the cytosol such as Ca21, when detected by Ca1-binding proteins or other NP-specific proteins. Tang et al. (2016) report an increase in the concentration of ROS in the A. thaliana L. root tissue exposed to Cu NPs. This increase is accompanied by a higher content of antioxidant compounds that maintain adequate ROS levels within cellular tissues. The increase of the enzymatic activity derived from NPs could be explained by the double function of NPs as essential nutrients and, at the same time, an enzymatic cofactor, or because of the exacerbation of the Haber
Weiss cycle (Raliya et al., 2015; Yanık and Vardar, 2015; Hou et al., 2018). NPs can be used for mitigating abiotic stress on crops, your application foliar, or/and addition to substrate/soil. Under abiotic stress the plant produces ROS and RNS minor quantity, generally these radicals are produced in chloroplast, mitochondria, peroxisoma or cytoplasm. For reduced of damage occasioned by ROS the plants active a system

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antioxidant to consume them. NPs could be increase ROS and also antioxidant capacity, in • this case NPs can be upturn a 1O2, O•, O2 2 , and a major quantity H2O2, OH radical is originate by NPs in the reaction Fenton in first case or Haber
Weiss reaction second case, because the transitional metal exacerbates these reactions on the plant. Radicals 1O2 and O• could be dissipated by action of α-tocopherol and β-carotene. SOD enzyme dismutes the O2 2 radical to H2 O 2, later CAT enzyme produce H 2 O and O 2 from peroxide hydrogen. H2O2 can be react with Cl2 and produce HOCl radical. And on the other hand, H2O2 is transformed to H2O by both enzymes GPX or APX, under your cycle respective, both needed energy how NADPH. H2O2 and O2 2 can enter the Fenton or Haber
Weiss reaction and produces •OH radical, in this case, ASH can be donator of electrons and stabilized them or produces by intrinsical reactions the molecules H2O and O2 (Fig. 13.2). 13.3.2.4.1 Enzyme compounds

Several studies report alterations in the plant enzymatic systems in response to NPs exposure. Yanık and Vardar (2015) mentioned that POD seems to be one of the enzymes, the role of which is considered significant to mitigate stress metabolism. They also indicate that the application of Al2O3 NPs on T. aestivum L. showed an initial increase in ROS, however, depending on the time of exposure to NPs, POD activity increased in the root. In Nicotiana tabacum L. there was an increase in the generation of ROS (MDA) in root and leaves, which could be dissipated by the activity of SOD, APX, CAT, and pyrogallol POD (PPX) enzymes induced by the application of Ag NPs (Cvjetko et al., 2018). Wang et al. (2016b) noticed an increase in the activity of enzymes as SOD, CAT, and POD by the presence of γ-Fe2O3 NPs in C. lanatus L. roots. Similarly, the application of Si NPs on corn and pea plants increased the enzymatic activity of SOD, APX, GR, and DHAR (Tripathi et al., 2015, 2016). In the case of saline stress conditions, it can be seen that the application of SiO2 NPs increased the enzymatic activity of CAT, POD, APX, and SOD in roots as well as in leaves of G. max L. (Farhangi-Abriz and Torabian, 2018). Mitigation

Crop under abiotic stress

ROS

Antioxidant capacity increase 1O

2–

O– SOD

NPs Fenton/Haber–Weiss reaction (transition metal) H2O + O2 •OH

Foliar

α-Tocopherol β-Carotene H2O + O2

CAT

O2•–

C1– HOCI

H2O2

Chloroplast ASH Mitochondria

NPs

Peroxisome

ROS Increase

H2O

APX MDA MDHAR ASH

DHA

DHAR GR

Substrate/soil

FIGURE 13.2

NADP+

GSSG GR

GSSG

GSH

H2O

GPX 2GSH

NADP+

NADPH

NADPH

Increase in antioxidant capacity induced by NPs mitigates abiotic stress in plants. NP,

Nanoparticles.

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Similarly, exposure to Al2O3 NPs in A. cepa L. plants considerably increases SOD activity, suggesting toxicity derived from the interaction with NPs (Rajeshwari et al., 2015). In Prosopis juliflora var. velutina roots, an increase in the enzymatic activity of APX and CAT exposed to CeO2 NPs was induced (Hernandez-Viezcas et al., 2016). The exposure of A. thaliana L. to Ag NPs induced a greater SOD, CAT, and POD activity in leaf tissues (Li et al., 2018). The application of ZnO NPs of in O. sativa L. increased SOD, CAT, APX, POD, GST, and DHAR enzymatic activity in a greater proportion in root than in leaves, which could lead to the dissipation of O2 2 , H2O 2 , and TBARS ROS (Singh et al., 2018). 13.3.2.4.2 Nonenzymatic compounds

Alterations in nonenzymatic systems of plants are reported in response to NPs exposure. Thiruvengadam et al. (2015) found an increase in H2O2 and MDA concentration, as well as a joint increase in anthocyanins levels under Ag NPs application in Brassica rapa ssp. Rapa L. On the other hand, exposure to TiO2 NPs induced the production of total tococromanols and α-tocopherol in A. thaliana L., which may lead to the reduction of lipid ´ peroxidation (Szymanska et al., 2016). Similarly, foliar application of ZnO NPs and Fe3O4 NPs on Moringa peregrina plants showed an increase in vitamin A and C content as well as carotenoids (Soliman et al., 2015). Samadi et al. (2015) reported an increase in carotenoid content, derived from an increase in ROS concentration, in Melissa officinalis L. exposed to TiO2 NPs. While Morteza et al. (2013) found that chlorophyll (a and b) content, carotenoids, and anthocyanins were increased in corn leaves exposed to TiO2 NPs. In another study by Li et al. (2018), Ag NPs increased the content of anthocyanins, which could mitigate the damage caused by the accumulation of ROS in the photosynthetic tissues of A. thaliana L. There was also an increase in GSH activity in the foliar tissues mitigating the damage caused by the excess of MDA. Farhangi-Abriz and Torabian (2018) reported in G. max L. under saline stress and with the application of SiO2 NPs that the content of phenolic compounds, ascorbic acid, and α-tocopherol were increased. A greater increase was observed related to a higher salinity condition. On the other hand, the use of Cu NPs adsorbed on Cs
PVA increased the content of total phenols and flavonoids in jalapeno peppers (Pinedo-Guerrero et al., 2017). Raliya et al. (2015) mention that the spraying of TiO2 and ZnO NPs on foliar tissue of tomato plants can increase chlorophyll content in leaves, as well as an increase in lycopene content in fruit. Similarly, Jua´rez-Maldonado et al. (2016), Herna´ndez-Herna´ndez et al. (2017), and Herna´ndez-Herna´ndez et al. (2018) reported an increase in carotene content in tomato fruits in plants exposed to Cu NPs adsorbed on Cs
PVA. On the other hand, Herna´ndez-Fuentes et al. (2017) and Herna´ndez-Herna´ndez et al. (2018) mentioned that Cu NPs application induce an accumulation of total phenols, β-carotene, and vitamin C in tomato fruits. On the other hand, oxidative stress generated by Ag NPs can induce an accumulation of several amino acids (aspartic acid, glutamic acid, serine, glycine, histidine, alanine, valine, proline, among others) as well as a SOD, CAT, and POD increase (Mehrian et al., 2015). This same response is reported by Veˇceˇrova´ et al. (2016) who applied CdO NPs on barley and found an increase in amino acid and organic acid concentrations in roots and leaves. Rossi et al. (2016) reported in B. napus L. developed under salinity stress

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conditions, that application of CeO2 NPs managed to increase the proline content. An increase in proline and phenolic compounds content in Rosmarinus officinalis L. is also reported when ZnO NPs are applied (Mohsenzadeh and Moosavian, 2017). 13.3.2.5 Induction of tolerance to abiotic stress through increased antioxidant capacity The antioxidant response generated by NPs will depend on the level of damage caused by ROS in the cells, as long as they do not reach phytotoxicity levels, and considering as well adequate levels of intracellular Ca21 (Marslin et al., 2017). When an increase in antioxidant compounds is generated, a positive response to abiotic stress will result, since, as previously mentioned, this induces ROS accumulation therefore generating oxidative stress. Different investigations have shown the induction of tolerance to different adverse environmental conditions through the application of NPs to crops (Table 13.1). The exposure of H. vulgare L. to NiO NPs presented an induction of anion O2 2 favoring oxidative stress and lipid peroxidation; however, the application of SiO2 NPs reduced the concentration of superoxide anion through the redox route of thiols (Soares et al., 2018). Cu NPs applied in S. lycopersicum L. and B. oleracea var. botrytis L. showed that the enzymatic activities of SOD and CAT were increased. This increase in enzymatic activity may mitigate the damage caused by excess lipid peroxidation (Singh et al., 2017). This same type of particles increased APX, CAT, SOD, and GPX activity as well as phenols, β-carotene, and vitamin C in S. lycopersicum L. leaves and fruits developed under saline stress (Herna´ndez-Fuentes et al., 2017). Ag NPs were able to mitigate the damage caused by flood and salinity in plants of G. max L. and O. sativa L. by increasing amino acids such as β-ketoacyl-reductase 1 as well as generating a greater CAT, SOD, APX, GR, and GPX enzymatic activity (Mustafa et al., 2016; Thuesombat et al., 2016). TiO2 NPs were able to mitigate cold stress by reducing H2O2 and MDA levels and increasing SOD, CAT, APX, and GPX activity in Cicer arietimun L. (Mohammadi et al., 2014). Similarly, chlorophyll and carotene content increased in Linum usitatissimum L. under drought conditions (Aghdam et al., 2016). Khan (2016) reported that these NPs increase SOD and POX activity besides total phenols in S. lycopersicum L. under salinity stress. It was possible to appreciate greater content of anthocyanins and CAT activity under drought conditions in O. basilicum L. when applying this type of NPs (Kiapour et al., 2015). In another study, higher proline content, which mitigates hydric stress, was found when NPs of TiO2 were applied in Dracocephalum moldavica L. (Mohammadi et al., 2016). The application of SiO2 NPs in Vicia faba L. developed under conditions of salinity stress increased CAT, APX, and POD enzymatic activity (Qados, 2015), while its application in Pisum sativum L. and Z. mays L. reduced ROS (O2 and H2O2) and lipid peroxidation protecting plants from heavy metal stress (Cr and AsV) by increasing CAT, SOD, GR, and DHAR activity and improving AsA
GSH cycle (Tripathi et al., 2015, 2016). S. lycopersicum L. plants under salinity conditions showed higher SOD and GPX activity when ZnO NPs were applied (Alharby et al., 2016a). On the other hand, Gowayed and Kadasa (2016) found a decrease in MDA and nitric oxide as well as an increase in SOD, GR, GPX, CAT, and GSH activity in V. faba L. under Cd stress. In M. peregrina, vitamins C

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TABLE 13.1

Application of nanoparticles (NPs) for abiotic stress management in plants.

NPs

Stress

Crop

Effect

References

TiO2

High light

Spinacia oleracea

Promoted photosynthesis and photochemical reaction of chloroplasts

Hong et al. (2005a)

TiO2

UV-B radiation

S. oleracea

Decrease in O2 2 , H2O2, and MDA. Increase in SOD, CAT, APX, GPX, and O2 in chloroplasts

Lei et al. (2008)

CeO2

HSP70 protein

Zea mays

Increase in the regulation of HSP70 protein to defend against oxidative injury

Zhao et al. (2012)

Ag

Flooding

Crocus sativus

Increase in the length of the root and dry weight Rezvani et al. of the leaves (2012)

TiO2

Cold

Cicer arietinum

Decrease in the electrolyte leakage rate and malondialdehyde content

Mohammadi et al. (2013)

TiO2

Drought

Triticum aestivum

Increase in agronomic characteristics, including the content of gluten and starch

Jaberzadeh et al. (2013)

ZnO

Drought

Glycine max

Increase in the rate and percentage of germination

Sedghi et al. (2013)

SiO2

Salinity

Solanum lycopersicum

Increase in germination rate, root length, and dry weight

Haghighi et al. (2012)

SiO2

Salinity

S. lycopersicum

Improved photosynthesis rate, mesophilic conductance and efficiency of water use

Haghighi and Pessarakli (2013)

TiO2

Heat

S. lycopersicum

Increase in photosynthetic efficiency

Qi et al. (2013)

TiO2

Cold

C. arietinum

Decreases H2O2 and MDA level, maintains stable chlorophylls and carotenoids, increases SOD, CAT, APX, and GPX

Mohammadi et al. (2014)

TiO2

Sequı´a

Ocimum basilicum

Increase in anthocyanin and CAT

Kiapour et al. (2015)

Ag

Flooding

G. max

Decrease in alcohol dehydrogenase 1 and pyruvate decarboxylase 2 genes

Mustafa et al. (2015a)

Low transcription level of glyoxalase II 3 Al2O3

Flooding

G. max

Increase in fresh weight and root length. Regulation in the synthesis/degradation of proteins of glycolysis and lipid metabolism

Mustafa et al. (2015b)

Cu

Deficit or toxicity

Vigna radiata

Increase in chlorophyll content

Pradhan et al. (2015)

Higher enzymatic activity NADP-GPDHase, FBPase, and RBPase Improves photosynthetic activity, increases assimilation N

SiO2

Salinity

Vicia faba

Increase in APX, CAT, and POD activity

Qados (2015) (Continued)

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TABLE 13.1 (Continued) NPs

Stress

Crop

Effect

References

SiO2

Salinity

V. faba

Increase in plant height, number of leaves, foliar area, fresh weight, and dry plant

Qados and Moftah (2015)

SiO2

Salinity

Lens culinaris

Improves germination percentage and bud length

Sabaghnia and Janmohammadi (2015)

ZnO
Fe3O4 Salinity

Moringa peregrina

Increase in vitamin C, E, POD, and SOD

Soliman et al. (2015)

SiO2

Capsicum annuum

Increases in plant height, fresh and dry leaf weight, and fruit weight

Tantawy et al. (2015)

Salinity

Increase in the content of N, P, and K SiO2

Heavy metals (Cr)

Pisum sativum

Reduces the radical O2 2 , H2O2, and lipid peroxidation

Tripathi et al. (2015)

Increase in CAT, SOD, GR, and DHAR activity Increase in content of Ca, K, Mg, P, B, Cu, Fe, and Zn in leaf and root

Lactuca sativa TiO2
Fe3O4 P availability

Increase in plant and root length, fresh air, and root weight

Zahra et al. (2015)

Greater biomass Increase in P concentration (leaf and root) Greater bioavailability of P in soil TiO2

Drought

Linum usitatissimum

Improved content of chlorophyll and carotenoids

Aghdam et al. (2016)

Decrease in the content of H2O2 and MDA ZnO

Salinity

S. lycopersicum

Increase in RNAm levels of SOD, and GPX

Alharby et al. (2016b)

ZnO

Salinity

S. lycopersicum

Increase SOD, and GPX

Alharby et al. (2016a)

P

Salinity

O. basilicum

Increase chlorophylls and P

Alipour (2016)

Ag

Salinity

S. lycopersicum

Upregulate of genes AREB, MAPK2, P5CS, and CRK1

Almutairi (2016a)

SiO2

Salinity

S. lycopersicum

Increase in germination percentage and germination rate of seeds, root length, and fresh weight

Almutairi (2016b)

Upregulate of genes AREB, TAS14, NCED3, and CRK1 (Continued)

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13.3 Impacts of nanoparticles in plants

TABLE 13.1

(Continued)

NPs

Stress

Crop

Effect

References

Fe2O3

Salinity

Mentha piperita

Increase in essential oil

Askary et al. (2016)

Increase of 1,8-cineol, cis-sabinene hydrate, germacrene D, and β-pinene ZnO

Heavy V. faba metal (Cd)

Ag

Drought

TiO2

Decrease in MDA and nitric oxide. Increase in SOD, GR, GPX, CAT, and GSH activity and vitamin C

Gowayed and Kadasa (2016)

L. culinaris

Increase in germination

Hojjat and Ganjali (2016)

Salinity

S. lycopersicum

Improved carbon anhydrase activity, nitrate reductase, SOD, POX. Increase in lycopene, total phenols, proline, and glycine betaine

Khan (2016)

TiO2

Hydric deficit

Dracocephalum moldavica

Higher proline content, reduction of H2O2, and MDA

Mohammadi et al. (2016)

Ag

Flooding

G. max

Increase in proteins related to amino acid synthesis (β-ketoacyl-reductase 1)

Mustafa et al. (2016)

Al2O3

Flooding

G. max

Increase in ribosomal proteins (isocitrate dehydrogenase)

Mustafa and Komatsu (2016)

Increase in mitochondrial membrane permeability ZnO

P deficit

V. radiata

Increase in phosphatase activity (acid and alkaline) and phytase

Raliya et al. (2016)

Greater absorption of P Better stem height, root volume, foliar protein, and chlorophyll content CeO2

Salinity

Brassica napus

Higher plant biomass and efficiency of the photosynthetic apparatus

Rossi et al. (2016)

Ag

Salinity

Oryza sativa

Greater CAT, SOD, APX, GR, and GPX activity

Thuesombat et al. (2016)

SiO2

Heavy metal (AsV)

Z. mays

Reduces toxicity

Tripathi et al. (2016)

CeO2

Salinity

B. napus

Greater biomass and photosynthetic efficiency

Rossi et al. (2017)

Cu

Salinity

S. lycopersicum

Increase in phenols, β-carotene, and vitamin C

Herna´ndezFuentes et al. (2017)

Fe2O3

Salinity

M. piperita

Decreased lipid peroxidation and proline

Askary et al. (2017)

Improved AsA
GSH cycle

(Continued)

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TABLE 13.1 (Continued) NPs

Stress

Crop

Effect

Fe3O4

Drought

Fragaria 3 ananassa Increase in growth and quality

Mozafari et al. (2018)

Cu

Salinity

S. lycopersicum

Herna´ndezHerna´ndez et al. (2018)

Increase in SOD, CAT, APX, GPX, PAL, lycopene, and vitamin C

References

APX, Ascorbate peroxidase; AsA
GSH, ascorbate
glutathione; CAT, catalase; DHAR, dehydroascorbate reductase; FBPase, fructose-1,6-bisphosphatase; GPDHase, glyceraldehyde-3-phosphate dehydrogenase; GPX, glutathione peroxidase; GR, glutathione reductase; HSP, heat-shock protein; MDA, malonaldehyde; RBPase, ribulose-5-phosphate kinase; SOD, superoxide dismutase; PAL, phenylalanine ammonia lyase.

and E content increased with a greater POD and SOD activity when applying ZnO NPs under salinity conditions (Soliman et al., 2015). Wu et al. (2017) mentioned that Ce NPs can eliminate ROS by catalyzing O2 2 , H2O2, and OH• radicals into oxygen, water, and hydroxyl ions, respectively, mitigating the damage caused by stress in A. thaliana L. under conditions of light, heat, or cold excess. It has been consistently observed that the increase in antioxidant capacity of plants is one of the main mechanisms used by NPs to induce tolerance to abiotic stress. This has been shown mainly for salinity stress; however, in other types of abiotic stress, such as cold, high radiation, drought, flooding, and heavy metals, NPs have also proved useful (Table 13.1).

13.3.3 Transcriptomic and proteomic responses of plants to nanoparticles and abiotic stress Transcriptomic and proteomic studies provide greater understanding at the molecular level of the effects generated by NPs in plants. It is known that both physiological and morphological effects depend to a large extent on the concentration applied, as well as on the size, shape, and type of NPs (Pe´rez-de-Luque, 2017). However, at a molecular level, there is less information about NPs induced modifications in plants, especially when plants support abiotic stress. As already described, several studies have shown that NPs induce tolerance to abiotic stress in different plant species (Khan et al., 2017). The transcriptomic and proteomic modifications of different plant species caused by the application of NPs, as well as their relationship with different abiotic stress conditions are shown later. 13.3.3.1 Transcriptomic modifications by nanoparticles and abiotic stress It was demonstrated that Ag NPs induce tolerance to salinity stress in tomato plants through the overexpression of AREB, MAPK2, P5CS, and CRK1 genes and the repression of the TAS14, DDF2, and ZFHD genes, these last ones involved in the regulation of abscisic acid (ABA) (Almutairi, 2016a). AREB gene is regulated by transcription factors such as AREB/ABF, which encode ABA and are crucial for inducing tolerance to osmotic stress, such as salinity stress and drought (Yoshida et al., 2015). MAPK2 gene, belonging to the family of MAP kinase genes, is of great importance since it participates in the regulation

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305

of the antioxidant and hormonal plant defense system in response to stress (Sinha et al., 2011) in conjunction with ROS and Ca21. The P5CS gene encodes proline biosynthesis, so its activation increases the ability of plants to tolerate both biotic and abiotic stresses (Rai and Penna, 2013). The repression of the TAS14 gene reduces the osmotic potential and increases the accumulation of solutes such as sugars and K1 allowing a greater tolerance to salinity stress and drought in plants (Mun˜oz-Mayor et al., 2012). On the other hand, the repression of the DDF2 gene increases the biosynthesis of gibberellic acid in plant organs (Lehti-Shiu et al., 2015). The repression of the ZFHD gene reduces the effects caused by drought and high salinity and is regulated by the biosynthesis of ABA (Figueiredo et al., 2012). In addition, Ag NPs induce tolerance in soybean plants under flood stress by repressing the alcohol dehydrogenase 1 and pyruvate decarboxylase 2 genes. There may be a relationship with cellular metabolism that is reflected in an increase in growth. On the other hand, the repression of the glyoxalases II 3 gene decreases the cytotoxicity of methylglyoxal, a result of glycolysis caused by flood stress (Mustafa et al., 2015a). In A. thaliana L., Ag NPs overexpress genes related to indoleacetic acid 8 (IAA8), 9-cisepoxycarotenoid dioxygenase (NCED3), and RD22 proteins in response to dehydration and repress ACC 7 synthase (ACS7) genes and ACC oxidase 2 (ACO2). These NPs are involved in different cellular processes, such as cell proliferation and photosynthesis, and also participate in hormonal signaling pathways, such as auxins, ABA, and ethylene (Syu et al., 2014). In B. rapa L., Ag NPs (5 and 10 mg/L) positively regulate the biosynthesis of glucosinolates and phenolic related genes, which are linked to abiotic and biotic stress, and repress carotenoids genes (Thiruvengadam et al., 2015). In A. thaliana L. Ag and Ag1 NPs overexpress genes mainly associated to metal response and oxidative stress, whereas the repressed genes were those regulated by auxins and ethylene. Three of the genes overexpressed by Ag NPs belong to the biosynthetic pathway of thalianol, which is believed participate in the plant’s antioxidant defense system (Kaveh et al., 2013). In cold-tolerant chickpea plants (Cicer arietinum L.), TiO2 NPs decrease transcription levels of CaLRubisco, CaSRubisco, and Cachlorophyll a/b genes after the sixth day of cold stress reaching control levels. This allows less oxidative damage in the photosynthetic structure, so TiO2 NPs ensure plant survival or recovery from cold stress. In addition, they could play an important role in the reduction of damage when the crop is developed in the field conditions, which translates into an increase in productivity (Hasanpour et al., 2015). Another transcriptomic study revealed that TiO2 NPs increase tolerance to cold stress in chickpea plants by activating different genes that are related to metabolic pathways, cellular defense systems, signaling mechanisms, and even in the regulation of transcription (Amini et al., 2017). Tumburu et al. (2017) mentioned that the TiO2 NPs specifically induce genes associated with photosynthesis in A. thaliana L., in such a way that NPs could induce stress tolerance by higher radiance. In Lactuca sativa L. plants treated with a combination of TiO2/ZnO NPs, hundreds of genes related to photosynthetic metabolism, antioxidant enzymes, metabolism of nitrogen and sucrose, and metabolic pathways of starch were identified (Wang et al., 2017). TiO2 NPs can act as gene regulators, since they affect the expression of microRNA profiles in N. tabacum L. It has also been shown to have an effect on the development of the plant, in addition to inducing tolerance to different environmental factors that can cause stress such as drought, salinity, and heavy metals (Frazier et al., 2014).

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Si NPs induced an increase in the expression of AREB, TAS14, NCED3, and CRK1 genes and a decrease in RBOH1, APX2, MAPK2, ERF5, MAPK3, and DDF2 genes in S. lycopersicum L. plants (Almutairi, 2016b). These genes are related to the biosynthesis of ABA and are activated by Si NPs, thus generating salinity stress tolerance. In O. sativa L. plants, Si NPs inhibit the expression of the genes OsLCT1 and OsNramp5 related to Cd uptake and transport and increase the expression of the genes OsHMA3 and OsLsi1 in the vacuole related to Cd transport and Si uptake, respectively. Thus Si NPs increased the absorption capacity of silicon and inhibited the absorption capacity of Cd, which resulted in relief of Cd toxicity (Cui et al., 2017). In Arabidopsis plants, application of 10 mg/L of CuO NPs modified the differential expression of 1658 genes, among which 1035 were positively regulated and 623 were negatively regulated. A total of 47 genes were regulated in response to oxidative stress, 19 genes participate in the stimulation responses by abiotic factors, and 12 genes are related to the KEGG metabolic pathway in the biosynthesis of phenylpropanoids. CuO NPs contributed much more strongly to the regulation of genes related to antioxidant system defense against oxidative stress than those corresponding to Cu21 ions (Tang et al., 2016). CuO NPs also positively increased the expression of genes that regulated auxin signaling and are essential to increase tolerance to abiotic stress in A. thaliana L. (AXR2/IAA7, AXR3/IAA17 and SLR1/IAA14). In addition, Fe-SOD gene, which is a chloroplastlocalized metalloenzyme that regulates oxidative stress, was increased your expression (Wang et al., 2016c). In C. pepo L., CuO NPs positively regulated BIP3 gene that encodes a heat-shock protein (HSP70), this is very important in the tolerance to high temperature, since it participates in the folding of proteins and therefore in their ability to remain stable (Pagano et al., 2017). In A. thaliana L. stressed by CuO NPs the expression of genes is related to different important functions as oxidative stress response, sulfur assimilation, and biosynthesis of nonenzymatic antioxidant compounds as GSH and proline (Nair and Chung, 2014). This results in greater tolerance to water or salinity stress. In Arabidopsis, ZnO NPs induce the expression of ontological genes related to both biotic and abiotic stresses, while repressing genes related to cell organization and biogenesis (Landa et al., 2012). In C. pepo L. the application of ZnO NPs regulated the expression of genes related to different stress conditions; 043d (PHT1; 1) gene related to heavy metal transport, 066u (AGL4) gene related to abiotic stress responses, 093u (Cutc008356) gene related to both biotic and abiotic stress, and 099u (NRT1.8) gene related to cadmium tolerance (Pagano et al., 2017). Other NPs, such as iron, enhance drought tolerance in A. thaliana L. by upregulating AHA2 gene expression, which is related to the control of closure and opening of stomata, which influences the adaptation to a drought stress condition (Kim et al., 2015). Cerium NPs induced the expression of genes related to activation of transcription factors belonging to the family of proteins binding to the ethylene sensitive element in A. thaliana L. (Tumburu et al., 2017). Different types and sizes of TiO2 NPs, Ag NPs, and carbon nanotubes repressed the expression of genes related to phosphate starvation responses as well as the inhibition of root hair development in A. thaliana L. (Garcı´a-Sa´nchez et al., 2015). Al2O3 NPs stimulated the transcription of genes related to root development and nutrition in Arabidopsis (Jin et al., 2017). All this information shows that NPs induce important modifications in the expression of genes related to tolerance to various types of abiotic

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307

FIGURE 13.3 Positive transcriptomic modifications induced by NPs to increase tolerance to abiotic stress in plants. Red arrows (black in print version) indicate an increase in tolerance to abiotic stress. NP, Nanoparticles.

stress (Fig. 13.3). Therefore this can be considered another mechanism for induction of stress tolerance by the application of NPs. 13.3.3.2 Proteomic modifications of plants exposed to nanoparticles In G. max L. plants Ag NPs has induced tolerance to flood stress through the positive regulation of β-ketoacyl-reductase 1 and increased proteins related to amino acid synthesis and to wax formation (Mustafa et al., 2016). Likewise, 107 differentially modified root proteins were detected and increase the tolerance to same conditions; these proteins are related to signaling and cell metabolism (Mustafa et al., 2015b). Another proteomic study showed that Ag NPs have positive effects on tolerance to oxidative stress in O. sativa L., due to regulation and signaling of Ca, protein transcription and degradation, cell wall synthesis, cell division, and apoptosis (Mirzajani et al., 2014). Moreover, the application of Ag NPs in Eruca sativa L. modified the expression of proteins that participate in redox regulation and sulfur metabolism (Vannini et al., 2013). Also, Ag NPs induce the expression of a small HSP in Daucus carota L. (Park et al., 2014). Thus this type of NPs could increase the tolerance to high temperature and high radiation in plants. Al2O3 NPs applied to G. max L. under flood stress regulate 172 common proteins; many of these are related to glycolysis and lipid metabolism, so they could regulate the metabolism of energy and cell death, which translates into greater tolerance to this condition of stress. Also some of these proteins are related to other processes as oxidation reduction, stress signaling, and hormonal pathways (Hossain et al., 2016). In wheat (Triticum spp. L.) varieties tolerant to

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FIGURE

13.4 Positive proteomic modifications induced by NPs in plants under conditions of abiotic stress. NP, Nanoparticles.

salinity and drought, the application of Cu NPs modified the starch degradation process, glycolysis, and the tricarboxylic acid cycle resulting in an increase in tolerance to stress (Yasmeen et al., 2017). Fe NPs improved the growth of wheat plants by increasing the abundance of proteins associated to photosynthesis in salt-tolerant varieties (Yasmeen et al., 2016). In kidney bean (P. vulgaris) a quantitative proteomic analysis shows that application of nanoceria upregulated proteins related to stress and downregulated proteins related to nutrient storage and carbohydrate metabolism (Majumdar et al., 2015). As observed, the application of NP induces modifications in the expression of proteins that finally relate to tolerance to different types of stress (Fig. 13.4). Therefore modification of protein expression may be another mechanism for the induction of tolerance to abiotic stress by NPs.

13.3.4 Positive effects of nanoparticles on agronomical aspects of crops As described, plants exposed to NPs trigger a series of mechanisms that can finally be translated into greater growth, development, and yield of plants (Du et al., 2017). This has been demonstrated in several recent studies, where NPs promote benefits for agricultural crops (Table 13.2). Several works have presented increases in plant vigor when applying NPs. Anandaraj and Natarajan (2017) showed increases in germination, bud and root length, and vigor index when coating seeds of A. cepa L. with 1000 mg/kg of ZnO, Ag, CuO, and TiO2 NPs. Afrayeem and Chaurasia (2017) reported that the application of ZnO NPs (0.75 g) promoted greater germination of seeds, as well as root, sprout, and plant length. Al2O3 NPs applied to A. thaliana L. promoted greater weight (48%) and larger roots (39%) and was related to the increase in the transcription of genes, which cause growth and absorption of nutrients from the roots, such as POLARIS protein (Jin et al., 2017).

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TABLE 13.2 (NPs).

Positive effects on the agronomic characteristics of plants by the application of nanoparticles

NPs

Crop

Effect

References

TiO2

Spinacia oleracea

Increases in the germination of aged seeds, increases vigor and growth

Zheng et al. (2005)

TiO2

S. oleracea

Increase in fresh and dry biomass

Yang et al. (2006)

TiO2

S. oleracea L.

Increased growth

Gao et al. (2008)

ZnO

Cicer arietinum

Greater germination and growth of the root of the seeds, increase in plant growth

Pandey et al. (2010)

CeO2

Triticum aestivum

Increase in plant height, aerial biomass, number of spikelets per spike, number of grains per spike and yield

Rico et al. (2014)

SiO2

Helianthus annuus

Increase in seed germination

Janmohammadi and Sabaghnia (2015)

CeO2

Hordeum vulgare

Increase in growth

Rico et al. (2015)

SiO2

Vicia faba

Increased germination, growth and flowering of plants

Roohizadeh et al. (2015)

Fe

T. aestivum

Increase in root weight and length and leaves

Yasmeen et al. (2016)

TiO2

Solanum lycopersicum

Increase in root length and plant height

Raliya et al. (2015)

Cu

S. lycopersicum

Increase in growth and performance

Jua´rez-Maldonado et al. (2016)

CeO2

S. lycopersicum

Increase in the number of fruits

Barrios et al. (2016)

Fe2O3

S. lycopersicum

Increase in germination, root length, and shoot

Shankramma et al. (2016)

CuO

Cucumis sativus

Increase in fruit weight

Hong et al. (2016)

CeO2

Brassica napus

Increase in biomass

Rossi et al. (2017)

Cu

S. lycopersicum

Increase in growth

Herna´ndezHerna´ndez et al. (2017)

Fe3O4

Fragaria

Increase in growth

Mozafari et al. (2018)

FeO

Oryza sativa

Increase in growth

Mankad et al. (2017)

Al2O3

Brassica oleracea

Increase in growth

Amist et al. (2017)

ZnO

Phaseolus vulgaris

Increase in root length and leaves

Medina-Velo et al. (2017) (Continued)

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TABLE 13.2 (Continued) NPs

Crop

Effect

References

ZnO

O. sativa

Increase in growth

Ruangthep et al. (2018)

Ca3(PO4)2

O. sativa

Increase in growth

Upadhyaya et al. (2017)

Nitrogen

Punica granatum

Increase in yield and number of fruits

Davarpanah et al. (2017)

ZnO, Ag, CuO, TiO2

Allium cepa

Increase in germination and vigor

Anandaraj and Natarajan (2017)

ZnO

O. sativa

Increase in growth and biomass

Singh et al. (2018)

Increase in germination and yield

Ramapuram et al. (2018)

ZnO, CaO, Sorghum MgO bicolor

Ruangthep et al. (2018) reported that ZnO NPs (200 mg/L) induced larger shoots (20.8%) and roots (23.4%), greater fresh (32.5%) and dry (49.6%) weight in O. sativa L., improving results as exposure time increased (30.6%, 39.2%, 88.9%, and 73.6%, respectively). The authors deduced a correlation between the increase produced by the NPs in photosynthetic pigments content and biomass. The use of Ce NPs combined with biochar improved plant height and foliar area of O. sativa L. and reduced P loss from surface water (Feng et al., 2017). The Ca3(PO4)2 NPs (20 mg/L) increased root (6%) and shoot (5%) length, fresh root (7%) and shoots (18%) biomass, dry root (11%), and buds (10%) biomass in O. sativa L. (Upadhyaya et al., 2017). Similarly, in L. usitatissimum L., under exposure of Fe2O3 NPs, greater seedling length, greater average number of seedlings with leaves, and larger roots were observed, possibly due to changes in POD and CAT metabolic activity (Karunakaran et al., 2017). Askary et al. (2017) showed that Fe2O3 NPs (30 μM) in Mentha piperita L. under salinity stress induced an increase in fresh and dry leaf biomass, because NPs are rapidly absorbed and provide the required nutrients. It also leads to a better Fe21/total Fe ratio in S. lycopersicum L. (Shankramma et al., 2016). Soil application of Fe3O4 NPs results in larger leaves and greater fresh biomass in B. napus L. under drought stress (Palmqvist et al., 2017). Kim et al. (2015) found that nano valent iron stimulates H1-ATPase activity inducing proton extrusion in the leaf apoplast, leading to cell wall expansion by turgor, as well as stomata opening, increasing CO2 in A. thaliana L. CeO2 NPs induced greater biomass in B. napus L. under drought stress (Rossi et al., 2016). Under the same stress in O. basilicum L., leaf fresh dry weight increased with the application of Si NPs (Kalteh et al., 2014). In C. pepo L., SiO2 NPs led to greater germination and seed growth, mediated by a lower concentration of MDA, H2O2, and loss of electrolytes (Siddiqui et al., 2014). Some studies showed an increase in agricultural crop production when applying NPs. Ramapuram et al. (2018) reported increases in grain yield (17.8% and 14.2%) and cane (7.2% and 8.0%) of Sorghum bicolor L., with ZnO, CaO, and MgO NPs treatment. Foliar and soil application of Zn NPs fertilizers led to increased yields and greater nutrient uptake in

Plant Life under Changing Environment

References

311

O. sativa L. (Apoorva et al., 2017). Jua´rez-Maldonado et al. (2016) reported an increase in diameter and greater stem dry weight (11% and 17%, respectively), as well as a greater number of fruits in S. lycopersicum L. when applying 0.006 mg/L of Cu NPs coated with chitosan. Similar results are presented by Pinedo-Guerrero et al. (2017), who reported a larger number of fruits per plant and greater total fruit weight in Capsicum annuum L. under exposure to Cu NPs in chitosan
PVA hydrogels. In another research, Herna´ndez-Herna´ndez et al. (2017) found that the application of 0.02, 2, and 10 mg of Cu NPs encapsulated in chitosan
PVA hydrogels improved development in S. lycopersicum L., with an increase in leaf number (5%), stem diameter, biomass fresh roots (25%), stem leaf dry biomass (13%) roots (30%), floral clusters (3%), and yield (17%). The authors suggested that NPs possibly mediated the increase in yield due to the greater accumulation of photosynthates in tomato fruits. In A. hypogaea L. the application of P NPs (2 and 4 mL/L) provided higher yields (Kumari et al., 2017). Wang et al. (2012) obtained higher yields (10%) when applying CeO2 NPs (10 mg/L), possibly due to greater energy transfer toward the fruit in S. lycopersicum L. Greater yield has been reported in S. bicolor L. grain with foliar and soil applications of ZnO NPs, under low and high levels of N, P, and K (Dimkpa et al., 2017). Under drought or high temperature stress, foliar application of SiO2 and TiO2 NPs led to an increase in grain weight, number of achenes per head, larger size, and achene performance in Helianthus annuus L., derived from a good source
demand relationship (Janmohammadi et al., 2017). Temperature can change the way in which ZnO NPs interact with plants, since at 25 C, concentrations of 100 and 800 mg/L increased root growth (22% and 27%) and at 30 C, 0.1 mg/L of Zn21 increased Z. mays L. growth by 50% (Lo´pez-Moreno et al., 2017).

13.4 Conclusion The application of different NPs in crops is a promising tool to induce tolerance to several types of abiotic stress. However, this depends on factors related to NPs characteristics (shape, size, dose, etc.), as well as crop type and application procedure. The induction of tolerance to abiotic stress by NPs is mainly caused by the increase of enzymatic and nonenzymatic antioxidant compounds that decrease oxidative stress in plants. However, it is clear that the application of NPs also modifies the expression of genes and proteins related to tolerance to abiotic stress. Therefore the tolerance induced by NPs themselves is a set of responses that encompass morphological, physiological, biochemical, genetic, and proteomic changes. This can be translated into positive effects on plant agronomic characteristics as greater vigor and yield, or else, in the increase of the quality of consumption organs.

References Adger, W.N., Dessai, S., Goulden, M., et al., 2009. Are there social limits to adaptation to climate change? Clim. Change 93, 335
354. Available from: https://doi.org/10.1007/s10584-008-9520-z. Afrayeem, S.M., Chaurasia, A.K., 2017. Effect of zinc oxide nanoparticles on seed germination and seed vigour in chilli (Capsicum annuum L.). J. Pharmacogn. Phytochem. 6, 1564
1566. Aghdam, M.T.B., Mohammadi, H., Ghorbanpour, M., 2016. Effects of nanoparticulate anatase titanium dioxide on physiological and biochemical performance of Linum usitatissimum (Linaceae) under well-watered and drought stress conditions. Rev. Bras. Bot. 39, 139
146. Available from: https://doi.org/10.1007/s40415-015-0227-x.

Plant Life under Changing Environment

312

13. Nanoparticles in plants: morphophysiological, biochemical, and molecular responses

Alharby, H., Metwali, E., Fuller, M., Aldhebiani, A., 2016a. Impact of application of zinc oxide nanoparticles on callus induction, plant regeneration, element content and antioxidant enzyme activity in tomato (Solanum lycopersicum Mill.) under salt stress. Arch. Biol. Sci. 68, 723
735. Available from: https://doi.org/10.2298/ ABS151105017A. Alharby, H.F., Metwali, E.M.R., Fuller, M.P., Aldhebiani, A.Y., 2016b. The alteration of mRNA expression of SOD and GPX genes, and proteins in tomato (Lycopersicon esculentum Mill) under stress of NaCl and/or ZnO nanoparticles. Saudi J. Biol. Sci. 23, 773
781. Available from: https://doi.org/10.1016/j.sjbs.2016.04.012. Alipour, Z.T., 2016. The effect of phosphorus and sulfur nanofertilizers on the growth and nutrition of Ocimum basilicum in response to salt stress. J. Chem. Health Risks 6, 125
131. Almutairi, Z.M., 2016a. Influence of silver nano-particles on the salt resistance of tomato (Solanum lycopersicum) during germination. Int. J. Agric. Biol. 18, 449
457. Available from: https://doi.org/10.17957/IJAB/15.0114. Almutairi, Z.M., 2016b. Effect of nano-silicon application on the expression of salt tolerance genes in germinating tomato (Solanum lycopersicum L.) seedlings under salt stress. Plant Omics 9, 106
114. Alves, T.F., Chaud, M.V., Grotto, D., et al., 2018. Association of silver nanoparticles and curcumin solid dispersion: antimicrobial and antioxidant properties. AAPS PharmSciTech 19, 225
231. Available from: https://doi. org/10.1208/s12249-017-0832-z. Amingad, V., Sreenivas, K.N., Fakrudin, B., et al., 2017. Comparison of silver nanoparticles and other metal nanoparticles on postharvest attributes and bacterial load in cut ros var. Taj Mahal. Int. J. Pure Appl. Biosci. 5, 579
584. Available from: https://doi.org/10.18782/2320-7051.2610. Amini, S., Maali-Amiri, R., Mohammadi, R., Kazemi- Shahandashti, S.S., 2017. cDNA-AFLP analysis of transcripts induced in chickpea plants by TiO2 nanoparticles during cold stress. Plant Physiol. Biochem. 111, 39
49. Available from: https://doi.org/10.1016/j.plaphy.2016.11.011. Amist, N., Singh, N.B., Yadav, K., et al., 2017. Comparative studies of Al31 ions and Al2O3 nanoparticles on growth and metabolism of cabbage seedlings. J. Biotechnol. 254, 1
8. Available from: https://doi.org/ 10.1016/j.jbiotec.2017.06.002. Anandaraj, K., Natarajan, N., 2017. Effect of nanoparticles for seed quality enhancement in onion [Allium cepa (Linn) cv. CO (On)] 5. Int. J. Curr. Microbiol. Appl. Sci. 6, 3714
3724. Available from: https://doi.org/ 10.20546/ijcmas.2017.611.435. Apoorva, M.R., Rao, P.C., Padmaja, G., 2017. Effect of zinc with special reference to nano zinc carrier on yield, nutrient content and uptake by rice (Oryza sativa L.). Int. J. Curr. Microbiol. Appl. Sci. 6, 1057
1063. Available from: https://doi.org/10.20546/ijcmas.2017.608.131. Arruda, C.S.C., Silva, D.A.L., Galazzi, M.R., et al., 2015. Nanoparticles applied to plant science: a review. Talanta 131, 693
705. Available from: https://doi.org/10.1016/j.talanta.2014.08.050. Asadapour, S., Madani, H., Mohammadi, G.N., et al., 2016. Control of high temperature stress in maize crop by nano-silicon and nano-zinc foliar application. Int. J. Trop. Agric. 34, 2213
2220. Ashour, H.A., Mahmoud, A.W.M., 2017. Response of Jatropha integerrima plants irrigated with different levels of saline water to nano silicon and gypsum. J. Agric. Stud. 5, 136
160. Available from: https://doi.org/10.5296/ jas.v5i4.12158. Askary, M., Talebi, S.M., Amini, F., Bangan, A.D.B., 2016. Effect of NaCl and iron oxide nanoparticles on Mentha piperita essential oil composition. Environ. Exp. Biol. 14, 27
32. Available from: https://doi.org/10.22364/ eeb.14.05. Askary, M., Talebi, S.M., Amini, F., Bangan, A.D., 2017. Effects of iron nanoparticles on Mentha piperita L. under salinity stress. Biologija 63, 65
75. Asli, S., Neumann, P.M., 2009. Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant, Cell Environ. 32, 577
584. Available from: https://doi.org/10.1111/j.1365-3040.2009.01952.x. Barrios, A.C., Rico, C.M., Trujillo-Reyes, J., et al., 2016. Effects of uncoated and citric acid coated cerium oxide nanoparticles, bulk cerium oxide, cerium acetate, and citric acid on tomato plants. Sci. Total Environ. 563
564, 956
964. Available from: https://doi.org/10.1016/j.scitotenv.2015.11.143. Baruah, S., Dutta, J., 2009. Nanotechnology applications in pollution sensing and degradation in agriculture. Environ. Chem. Lett. 7, 191
204. Available from: https://doi.org/10.1007/s10311-009-0228-8. Biswas, P., Wu, C.-Y., 2005. Nanoparticles and the environment. J. Air Waste Manage. Assoc. 55, 708
746. Available from: https://doi.org/10.1080/10473289.2005.10464656.

Plant Life under Changing Environment

References

313

Boghossian, A.A., Sen, F., Gibbons, B.M., et al., 2013. Application of nanoparticle antioxidants to enable hyperstable chloroplasts for solar energy harvesting. Adv. Energy Mater. 3, 881
893. Available from: https:// doi.org/10.1002/aenm.201201014. ´ Byczynska, A., 2017. Improvement of postharvest quality of cut tulip “White Parrot” by nano silver. World Sci. News 83, 224
228. Byrt, C.S., Munns, R., Burton, R.A., et al., 2018. Root cell wall solutions for crop plants in saline soils. Plant Sci. 269, 47
55. Available from: https://doi.org/10.1016/j.plantsci.2017.12.012. Cai, F., Wu, X., Zhang, H., et al., 2017. Impact of TiO2 nanoparticles on lead uptake and bioaccumulation in rice (Oryza sativa L.). NanoImpact 5, 101
108. Available from: https://doi.org/10.1016/j.impact.2017.01.006. Chellaram, C., Murugaboopathi, G., John, A.A., et al., 2014. Significance of nanotechnology in food industry. APCBEE Procedia 8, 109
113. Available from: https://doi.org/10.1016/j.apcbee.2014.03.010. Cheng, C.J., Tietjen, G.T., Saucier-Sawyer, J.K., Saltzman, W.M., 2015. A holistic approach to targeting disease with polymeric nanoparticles. Nat. Rev. Drug Discovery 14, 239
247. Available from: https://doi.org/ 10.1038/nrd4503. Clark, M., Tilman, D., 2017. Comparative analysis of environmental impacts of agricultural production systems, agricultural input efficiency, and food choice. Environ. Res. Lett. 12, 64016. Available from: https://doi.org/ 10.1088/1748-9326/aa6cd5. Corredor, E., Testillano, P.S., Coronado, M.-J., et al., 2009. Nanoparticle penetration and transport in living pumpkin plants: in situ subcellular identification. BMC Plant Biol. 9, 45. Available from: https://doi.org/10.1186/ 1471-2229-9-45. Couto, N., Wood, J., Barber, J., 2016. The role of glutathione reductase and related enzymes on cellular redox homoeostasis network. Free Radical Biol. Med. 95, 27
42. Available from: https://doi.org/10.1016/j. freeradbiomed.2016.02.028. Cui, J., Liu, T., Li, F., et al., 2017. Silica nanoparticles alleviate cadmium toxicity in rice cells: mechanisms and size effects. Environ. Pollut. 228, 363
369. Available from: https://doi.org/10.1016/j.envpol.2017.05.014. ˇ Cvjetko, P., Zovko, M., Stefani´ c, P.P., et al., 2018. Phytotoxic effects of silver nanoparticles in tobacco plants. Environ. Sci. Pollut. Res. 25, 5590
5602. Available from: https://doi.org/10.1007/s11356-017-0928-8. Da Costa, M.V.J., Sharma, P.K., 2016. Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica 54, 110
119. Available from: https://doi.org/ 10.1007/s11099-015-0167-5. Davarpanah, S., Tehranifar, A., Davarynejad, G., et al., 2017. Effects of foliar nano-nitrogen and urea fertilizers on the physical and chemical properties of pomegranate (Punica granatum cv. Ardestani) fruits. HortScience 52, 288
294. Available from: https://doi.org/10.21273/HORTSCI11248-16. Dimkpa, C.O., White, J.C., Elmer, W.H., Gardea-Torresdey, J., 2017. Nanoparticle and ionic Zn promote nutrient loading of sorghum grain under low NPK fertilization. J. Agric. Food Chem. 65, 8552
8559. Available from: https://doi.org/10.1021/acs.jafc.7b02961. Dittberner, H., Korte, A., Weber, A.P.M., Monroe, G., 2018. Natural variation in stomata size contributes to the local adaptation of water-use efficiency in Arabidopsis thaliana. bioRxiv 253021. Available from: https://doi. org/10.1101/253021. Du, W., Tan, W., Peralta-Videa, J.R., et al., 2017. Interaction of metal oxide nanoparticles with higher terrestrial plants: physiological and biochemical aspects. Plant Physiol. Biochem. 110, 210
225. Available from: https:// doi.org/10.1016/j.plaphy.2016.04.024. Duhan, J.S., Kumar, R., Kumar, N., et al., 2017. Nanotechnology: the new perspective in precision agriculture. Biotechnol. Rep. 15, 11
23. Available from: https://doi.org/10.1016/j.btre.2017.03.002. Fakoya, M.F., Shah, S.N., 2017. Emergence of nanotechnology in the oil and gas industry: emphasis on the application of silica nanoparticles. Petroleum 3, 391
405. Available from: https://doi.org/10.1016/j. petlm.2017.03.001. Farhangi-Abriz, S., Torabian, S., 2018. Nano-silicon alters antioxidant activities of soybean seedlings under salt toxicity. Protoplasma 1
10. Available from: https://doi.org/10.1007/s00709-017-1202-0. Feng, Y., Lu, H., Liu, Y., et al., 2017. Nano-cerium oxide functionalized biochar for phosphate retention: preparation, optimization and rice paddy application. Chemosphere 185, 816
825. Available from: https://doi.org/ 10.1016/j.chemosphere.2017.07.107.

Plant Life under Changing Environment

314

13. Nanoparticles in plants: morphophysiological, biochemical, and molecular responses

Figueiredo, D.D., Barros, P.M., Cordeiro, A.M., et al., 2012. Seven zinc-finger transcription factors are novel regulators of the stress responsive gene OsDREB1B. J. Exp. Bot. 63, 3643
3656. Available from: https://doi.org/ 10.1093/jxb/ers035. Frazier, T.P., Burklew, C.E., Zhang, B., 2014. Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum). Funct. Integr. Genomics 14, 75
83. Available from: https://doi.org/ 10.1007/s10142-013-0341-4. Gallocchio, F., Belluco, S., Ricci, A., 2015. Nanotechnology and food: brief overview of the current scenario. Procedia Food Sci. 5, 85
88. Available from: https://doi.org/10.1016/j.profoo.2015.09.022. Gao, F., Liu, C., Qu, C., et al., 2008. Was improvement of spinach growth by nano-TiO2 treatment related to the changes of Rubisco activase? BioMetals 21, 211
217. Available from: https://doi.org/10.1007/s10534-0079110-y. Garcı´a-Sa´nchez, S., Bernales, I., Cristobal, S., 2015. Early response to nanoparticles in the Arabidopsis transcriptome compromises plant defence and root-hair development through salicylic acid signalling. BMC Genomics 16, 341. Available from: https://doi.org/10.1186/s12864-015-1530-4. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909
930. Available from: https://doi.org/10.1016/j.plaphy.2010.08.016. Gonza´lez-Go´mez, H., Ramı´rez-Godina, F., Ortega-Ortiz, H., et al., 2017. Use of chitosan-PVA hydrogels with copper nanoparticles to improve the growth of grafted watermelon. Molecules 22, 1031. Available from: https:// doi.org/10.3390/molecules22071031. Gowayed, S.M., Kadasa, N.M., 2016. Effect of zinc oxide nanoparticles on antioxidative system of faba bean (Vicia faba L.) seedling expose to cadmium. Life Sci. J. 13, 18
27. Available from: https://doi.org/10.7537/ marslsj13031603.Key. Haghighi, M., Pessarakli, M., 2013. Influence of silicon and nano-silicon on salinity tolerance of cherry tomatoes (Solanum lycopersicum L.) at early growth stage. Sci. Hortic. (Amsterdam) 161, 111
117. Available from: https://doi.org/10.1016/j.scienta.2013.06.034. Haghighi, M., Afifipour, Z., Mozafarian, M., 2012. The effect of N-Si on tomato seed germination under salinity levels. J. Biol. Environ. Sci. 6, 87
90. Hasanpour, H., Maali-Amir, R., Zeinali, H., 2015. Effect of TiO2 nanoparticles on metabolic limitations to photosynthesis under cold in chickpea. Russ. J. Plant Physiol. 62, 779
787. Available from: https://doi.org/ 10.1134/S1021443715060096. Herna´ndez-Fuentes, A., Lo´pez-Vargas, E., Pinedo-Espinoza, J., et al., 2017. Postharvest behavior of bioactive compounds in tomato fruits treated with Cu nanoparticles and NaCl stress. Appl. Sci. 7, 980. Available from: https://doi.org/10.3390/app7100980. Herna´ndez-Herna´ndez, H., Benavides-Mendoza, A., Ortega-Ortiz, H., et al., 2017. Cu nanoparticles in chitosanPVA hydrogels as promoters of growth, productivity and fruit quality in tomato. Emirates J. Food Agric. 29, 573
580. Available from: https://doi.org/10.9755/ejfa.2016-08-1127. Herna´ndez-Herna´ndez, H., Gonza´lez-Morales, S., Benavides-Mendoza, A., et al., 2018. Effects of chitosan
PVA and Cu nanoparticles on the growth and antioxidant capacity of tomato under saline stress. Molecules 23, 178. Available from: https://doi.org/10.3390/molecules23010178. Hernandez-Viezcas, J.A., Castillo-Michel, H., Peralta-Videa, J.R., Gardea-Torresdey, J.L., 2016. Interactions between CeO2 nanoparticles and the desert plant mesquite: a spectroscopy approach. ACS Sustain. Chem. Eng. 4, 1187
1192. Available from: https://doi.org/10.1021/acssuschemeng.5b01251. Hojjat, S.S., Ganjali, A., 2016. The effect of silver nanoparticle on lentil seed germination under drought stress. Int. J. Farming Allied Sci. 5, 208
212. Hong, E., Dobrovolskaia, M.A., 2018. Addressing barriers to effective cancer immunotherapy with nanotechnology: achievements, challenges, and roadmap to the next generation of nanoimmunotherapeutics. Adv. Drug Delivery Rev. Available from: https://doi.org/10.1016/j.addr.2018.01.005. Hong, F., Yang, F., Liu, C., et al., 2005a. Influences of nano-TiO2 on the chloroplast aging of spinach under light. Biol. Trace Elem. Res. 104, 249
260. Available from: https://doi.org/10.1385/BTER:104:3:249. Hong, F., Zhou, J., Liu, C., et al., 2005b. Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach. Biol. Trace Elem. Res. 105, 269
280. Available from: https://doi.org/10.1385/BTER:105:1-3:269.

Plant Life under Changing Environment

References

315

Hong, J., Wang, L., Sun, Y., et al., 2016. Foliar applied nanoscale and microscale CeO2 and CuO alter cucumber (Cucumis sativus) fruit quality. Sci. Total Environ. 563
564, 904
911. Available from: https://doi.org/10.1016/ j.scitotenv.2015.08.029. Hossain, Z., Mustafa, G., Sakata, K., Komatsu, S., 2016. Insights into the proteomic response of soybean towards Al2O3, ZnO, and Ag nanoparticles stress. J. Hazard. Mater. 304, 291
305. Available from: https://doi.org/ 10.1016/j.jhazmat.2015.10.071. Hou, J., Wu, Y., Li, X., et al., 2018. Toxic effects of different types of zinc oxide nanoparticles on algae, plants, invertebrates, vertebrates and microorganisms. Chemosphere 193, 852
860. Available from: https://doi.org/ 10.1016/j.chemosphere.2017.11.077. Huang, Q., Wang, Y., Chen, X., et al., 2018. Nanotechnology-based strategies for early cancer diagnosis using circulating tumor cells as a liquid biopsy. Nanotheranostics 2, 21
41. Available from: https://doi.org/10.7150/ ntno.22091. Jaberzadeh, A., Moaveni, P., Tohidi Moghadam, H.R., Zahedi, H., 2013. Influence of bulk and nanoparticles titanium foliar application on some agronomic traits, seed gluten and starch contents of wheat subjected to water deficit stress. Not. Bot. Horti Agrobot. Cluj-Napoca 41, 201
207. Available from: https://doi.org/10.15835/ NBHA4119093. Janmohammadi, M., Sabaghnia, N., 2015. Effect of pre-sowing seed treatments with silicon nanoparticles on germinability of sunflower (Helianthus annuus). Bot. Lith. 21, 13
21. Available from: https://doi.org/10.1515/ botlit-2015-0002. Janmohammadi, M., Yousefzadeh, S., Dashti, S., Sabaghnia, N., 2017. Effects of exogenous application of nano particles and compatible organic solutes on sunflower (Helianthus annuus L.). Bot. Serbica 41, 37
46. Available from: https://doi.org/10.5281/zenodo.453554. Jasinski, D., Haque, F., Binzel, D.W., Guo, P., 2017. Advancement of the emerging field of RNA nanotechnology. ACS Nano 11, 1142
1164. Available from: https://doi.org/10.1021/acsnano.6b05737. Jin, Y., Fan, X., Li, X., et al., 2017. Distinct physiological and molecular responses in Arabidopsis thaliana exposed to aluminum oxide nanoparticles and ionic aluminum. Environ. Pollut. 228, 517
527. Available from: https:// doi.org/10.1016/j.envpol.2017.04.073. Jo´sko, I., Oleszczuk, P., Skwarek, E., 2017. Toxicity of combined mixtures of nanoparticles to plants. J. Hazard. Mater. 331, 200
209. Available from: https://doi.org/10.1016/j.jhazmat.2017.02.028. Jua´rez-Maldonado, A., Ortega-Ortı´z, H., Pe´rez-Labrada, F., et al., 2016. Cu nanoparticles absorbed on chitosan hydrogels positively alter morphological, production, and quality characteristics of tomato. J. Appl. Bot. Food Qual. 89, 183
189. Available from: https://doi.org/10.5073/JABFQ.2016.089.023. Kalteh, M., Alipour, Z.T., Ashraf, S., et al., 2014. Effect of silica nanoparticles on basil (Ocimum basilicum) under salinity stress. J. Chem. Health Risks 4, 49
55. Karunakaran, G., Jagathambal, M., Van Minh, N., et al., 2017. Green synthesized iron oxide nanoparticles: a nanonutrient for the growth and enhancement of flax (Linum usitatissimum L.) plant. Int. J. Biotechnol. Bioeng. 11, 289
293. Kaveh, R., Li, Y.-S., Ranjbar, S., et al., 2013. Changes in Arabidopsis thaliana gene expression in response to silver nanoparticles and silver ions. Environ. Sci. Technol. 47, 10637
10644. Available from: https://doi.org/ 10.1021/es402209w. Khan, M.N., 2016. Nano-titanium dioxide (nano-TiO2) mitigates NaCl stress by enhancing antioxidative enzymes and accumulation of compatible solutes in tomato (Lycopersicon esculentum Mill.). J. Plant Sci. 11, 1
11. Available from: https://doi.org/10.3923/jps.2016.1.11. Khan, M.N., Mobin, M., Abbas, Z.K., et al., 2017. Role of nanomaterials in plants under challenging environments. Plant Physiol. Biochem. 110, 194
209. Available from: https://doi.org/10.1016/j.plaphy.2016.05.038. Kiapour, H., Moaveni, P., Habibi, D., Sani, B., 2015. Evaluation of the application of gibberellic acid and titanium dioxide nanoparticles under drought stress on some traits of basil (Ocimum basilicum L.). Int. J. Agron. Agric. Res. 6, 138
150. Kim, J.-H., Oh, Y., Yoon, H., et al., 2015. Iron nanoparticle-induced activation of plasma membrane H 1 -ATPase promotes stomatal opening in Arabidopsis thaliana. Environ. Sci. Technol. 49, 1113
1119. Available from: https://doi.org/10.1021/es504375t.

Plant Life under Changing Environment

316

13. Nanoparticles in plants: morphophysiological, biochemical, and molecular responses

Kim, D.-Y., Kadam, A., Shinde, S., et al., 2018. Recent developments in nanotechnology transforming the agricultural sector: a transition replete with opportunities. J. Sci. Food Agric. 98, 849
864. Available from: https:// doi.org/10.1002/jsfa.8749. Kosova´, K., Vı´ta´mva´s, P., Urban, M., et al., 2018. Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. Front. Plant Sci. 9. Available from: https://doi.org/10.3389/fpls.2018.00122. Kumari, A., Yadav, S.K., 2014. Nanotechnology in agri-food sector. Crit. Rev. Food Sci. Nutr. 54, 975
984. Available from: https://doi.org/10.1080/10408398.2011.621095. Kumari, M.S., Rao, P.C., Padmaja, G., et al., 2017. Effect of bio and nano phosphorus on yield, yield attributes and oil content of groundnut (Arachis hypogaea L.). Environ. Conserv. J. 18, 21
26. Labunskyy, V.M., Hatfield, D.L., Gladyshev, V.N., 2014. Selenoproteins: molecular pathways and physiological roles. Physiol. Rev. 94, 739
777. Available from: https://doi.org/10.1152/physrev.00039.2013. Landa, P., Vankova, R., Andrlova, J., et al., 2012. Nanoparticle-specific changes in Arabidopsis thaliana gene expression after exposure to ZnO, TiO2, and fullerene soot. J. Hazard. Mater. 241
242, 55
62. Available from: https://doi.org/10.1016/j.jhazmat.2012.08.059. Lehti-Shiu, M.D., Uygun, S., Moghe, G.D., et al., 2015. Molecular evidence for functional divergence and decay of a transcription factor derived from whole-genome duplication in Arabidopsis thaliana. Plant Physiol. 168, 1717
1734. Available from: https://doi.org/10.1104/pp.15.00689. Lei, Z., Mingyu, S., Chao, L., et al., 2007. Effects of nanoanatase TiO2 on photosynthesis of spinach chloroplasts under different light illumination. Biol. Trace Elem. Res. 119, 68
76. Available from: https://doi.org/10.1007/ s12011-007-0047-3. Lei, Z., Mingyu, S., Xiao, W., et al., 2008. Antioxidant stress is promoted by nano-anatase in spinach chloroplasts under UV-B radiation. Biol. Trace Elem. Res. 121, 69
79. Available from: https://doi.org/10.1007/s12011-0078028-0. Le Ouay, B., Stellacci, F., 2015. Antibacterial activity of silver nanoparticles: a surface science insight. Nano Today 10, 339
354. Available from: https://doi.org/10.1016/j.nantod.2015.04.002. Li, J., Hu, J., Xiao, L., et al., 2017. Physiological effects and fluorescence labeling of magnetic iron oxide nanoparticles on citrus (Citrus reticulata) seedlings. Water Air Soil Pollut. 228, 52. Available from: https://doi.org/ 10.1007/s11270-016-3237-9. Li, X., Ke, M., Zhang, M., et al., 2018. The interactive effects of diclofop-methyl and silver nanoparticles on Arabidopsis thaliana: growth, photosynthesis and antioxidant system. Environ. Pollut. 232, 212
219. Available from: https://doi.org/10.1016/j.envpol.2017.09.034. Lin, D., Xing, B., 2008. Root uptake and phytotoxicity of ZnO nanoparticles. Environ. Sci. Technol. 42, 5580
5585. Available from: https://doi.org/10.1021/es800422x. Liu, R., Lal, R., 2015. Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Sci. Total Environ. 514, 131
139. Available from: https://doi.org/10.1016/j.scitotenv.2015.01.104. Lo´pez-Moreno, M.L., de la Rosa, G., Cruz-Jime´nez, G., et al., 2017. Effect of ZnO nanoparticles on corn seedlings at different temperatures; X-ray absorption spectroscopy and ICP/OES studies. Microchem. J. 134, 54
61. Available from: https://doi.org/10.1016/j.microc.2017.05.007. Ma, X., Geiser-Lee, J., Deng, Y., Kolmakov, A., 2010. Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci. Total Environ. 408, 3053
3061. Available from: https:// doi.org/10.1016/j.scitotenv.2010.03.031. Ma, Y., He, X., Zhang, P., et al., 2017. Xylem and phloem based transport of CeO2 nanoparticles in hydroponic cucumber plants. Environ. Sci. Technol. 51, 5215
5221. Available from: https://doi.org/10.1021/acs. est.6b05998. Majumdar, S., Almeida, I.C., Arigi, E.A., et al., 2015. Environmental effects of nanoceria on seed production of common bean (Phaseolus vulgaris): a proteomic analysis. Environ. Sci. Technol. 49, 13283
13293. Available from: https://doi.org/10.1021/acs.est.5b03452. Mallick, K., Witcomb, M., Scurrell, M., 2006. Silver nanoparticle catalysed redox reaction: an electron relay effect. Mater. Chem. Phys. 97, 283
287. Available from: https://doi.org/10.1016/j.matchemphys.2005.08.011. Mankad, M., Fougat, R.S., Patel, A., et al., 2017. Assessment of physiological and biochemical changes in rice seedlings exposed to bulk and nano iron particles. Int. J. Pure Appl. Biosci. 5, 150
159. Available from: https:// doi.org/10.18782/2320-7051.2818.

Plant Life under Changing Environment

References

317

Marslin, G., Sheeba, C.J., Franklin, G., 2017. Nanoparticles alter secondary metabolism in plants via ROS burst. Front. Plant Sci. 8. Available from: https://doi.org/10.3389/fpls.2017.00832. McNeil, S.E., 2005. Nanotechnology for the biologist. J. Leukocyte Biol. 78, 585
594. Available from: https://doi. org/10.1189/jlb.0205074. Medina-Velo, I.A., Barrios, A.C., Zuverza-Mena, N., et al., 2017. Comparison of the effects of commercial coated and uncoated ZnO nanomaterials and Zn compounds in kidney bean (Phaseolus vulgaris) plants. J. Hazard. Mater. 332, 214
222. Available from: https://doi.org/10.1016/j.jhazmat.2017.03.008. Mehrian, S.K., Heidari, R., Rahmani, F., 2015. Effect of silver nanoparticles on free amino acids content and antioxidant defense system of tomato plants. Indian J. Plant Physiol. 20, 257
263. Available from: https://doi. org/10.1007/s40502-015-0171-6. Mirzajani, F., Askari, H., Hamzelou, S., et al., 2014. Proteomics study of silver nanoparticles toxicity on Oryza sativa L. Ecotoxicol. Environ. Saf. 108, 335
339. Available from: https://doi.org/10.1016/j.ecoenv.2014.07.013. Mishra, S., Keswani, C., Abhilash, P.C., et al., 2017. Integrated approach of agri-nanotechnology: challenges and future trends. Front. Plant Sci. 8. Available from: https://doi.org/10.3389/fpls.2017.00471. Mohammadbagheri, L., Naderi, D., 2017. Effect of growth medium and calcium nano-fertilizer on quality and some characteristics of gerbera cut flower. J. Ornam. Plants 7, 205
212. Mohammed, L., Gomaa, H.G., Ragab, D., Zhu, J., 2017. Magnetic nanoparticles for environmental and biomedical applications: a review. Particuology 30, 1
14. Available from: https://doi.org/10.1016/ j.partic.2016.06.001. Mohammadi, R., Maali-Amiri, R., Abbasi, A., 2013. Effect of TiO2 nanoparticles on chickpea response to cold stress. Biol. Trace Elem. Res. 152, 403
410. Available from: https://doi.org/10.1007/s12011-013-9631-x. Mohammadi, R., Maali-Amiri, R., Mantri, N.L., 2014. Effect of TiO2 nanoparticles on oxidative damage and antioxidant defense systems in chickpea seedlings during cold stress. Russ. J. Plant Physiol. 61, 768
775. Available from: https://doi.org/10.1134/S1021443714050124. Mohammadi, H., Esmailpour, M., Gheranpaye, A., 2016. Effects of TiO2 nanoparticles and water-deficit stress on morpho-physiological characteristics of dragonhead (Dracocephalum moldavica L.) plants. Acta Agric. Slov. 107, 385. Available from: https://doi.org/10.14720/aas.2016.107.2.11. Mohsenzadeh, S., Moosavian, S.S., 2017. Zinc sulphate and nano-zinc oxide effects on some physiological parameters of Rosmarinus officinalis. Am. J. Plant Sci. 8, 2635
2649. Available from: https://doi.org/10.4236/ ajps.2017.811178. Monica, R.C., Cremonini, R., 2009. Nanoparticles and higher plants. Caryologia 62, 161
165. Available from: https://doi.org/10.1080/00087114.2004.10589681. Morteza, E., Moaveni, P., Farahani, H., Kiyani, M., 2013. Study of photosynthetic pigments changes of maize (Zea mays L.) under nano TiO2 spraying at various growth stages. Springerplus 2, 247. Available from: https://doi. org/10.1186/2193-1801-2-247. Mozafari, A.A., Havas, F., Ghaderi, N., 2018. Application of iron nanoparticles and salicylic acid in in vitro culture of strawberries (Fragaria 3 ananassa Duch.) to cope with drought stress. Plant Cell Tissue Organ Cult. 132, 511
523. Available from: https://doi.org/10.1007/s11240-017-1347-8. Mun˜oz-Mayor, A., Pineda, B., Garcia-Abella´n, J.O., et al., 2012. Overexpression of dehydrin tas14 gene improves the osmotic stress imposed by drought and salinity in tomato. J. Plant Physiol. 169, 459
468. Available from: https://doi.org/10.1016/j.jplph.2011.11.018. Mustafa, G., Komatsu, S., 2016. Insights into the response of soybean mitochondrial proteins to various sizes of aluminum oxide nanoparticles under flooding stress. J. Proteome Res. 15, 4464
4475. Available from: https:// doi.org/10.1021/acs.jproteome.6b00572. Mustafa, G., Sakata, K., Hossain, Z., Komatsu, S., 2015a. Proteomic study on the effects of silver nanoparticles on soybean under flooding stress. J. Proteomics 122, 100
118. Available from: https://doi.org/10.1016/ j.jprot.2015.03.030. Mustafa, G., Sakata, K., Komatsu, S., 2015b. Proteomic analysis of flooded soybean root exposed to aluminum oxide nanoparticles. J. Proteomics 128, 280
297. Available from: https://doi.org/10.1016/j.jprot.2015.08.010. Mustafa, G., Sakata, K., Komatsu, S., 2016. Proteomic analysis of soybean root exposed to varying sizes of silver nanoparticles under flooding stress. J. Proteomics 148, 113
125. Available from: https://doi.org/10.1016/ j.jprot.2016.07.027.

Plant Life under Changing Environment

318

13. Nanoparticles in plants: morphophysiological, biochemical, and molecular responses

Naderi, N., Karponis, D., Mosahebi, A., Seifalian, A.M., 2018. Nanoparticles in wound healing; from hope to promise, from promise to routine. Front. Biosci. (Landmark Ed. 23, 1038
1059. Available from: https://doi. org/10.2741/4632. Nair, P.M.G., Chung, I.M., 2014. Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignificaion, and molecular level changes. Environ. Sci. Pollut. Res. 21, 12709
12722. Available from: https://doi.org/10.1007/s11356-014-3210-3. Nair, P.M.G., Chung, I.M., 2015. Physiological and molecular level studies on the toxicity of silver nanoparticles in germinating seedlings of mung bean (Vigna radiata L.). Acta Physiol. Plant. 37, 1719. Available from: https://doi.org/10.1007/s11738-014-1719-1. Nair, R., Varghese, S.H., Nair, B.G., et al., 2010. Nanoparticulate material delivery to plants. Plant Sci. 179, 154
163. Available from: https://doi.org/10.1016/j.plantsci.2010.04.012. Nummelin, S., Kommeri, J., Kostiainen, M.A., Linko, V., 2018. Evolution of structural DNA nanotechnology. Adv. Mater. 30. Available from: https://doi.org/10.1002/adma.201703721. Pagano, L., Pasquali, F., Majumdar, S., et al., 2017. Exposure of Cucurbita pepo to binary combinations of engineered nanomaterials: physiological and molecular response. Environ. Sci. Nano 4, 1579
1590. Available from: https://doi.org/10.1039/C7EN00219J. Palmqvist, N.G.M., Seisenbaeva, G.A., Svedlindh, P., Kessler, V.G., 2017. Maghemite nanoparticles acts as nanozymes, improving growth and abiotic stress tolerance in Brassica napus. Nanoscale Res. Lett. 12, 631. Available from: https://doi.org/10.1186/s11671-017-2404-2. Pandey, A.C., Sanjay, S.S., Yadav, R.S., 2010. Application of ZnO nanoparticles in influencing the growth rate of Cicer arietinum. J. Exp. Nanosci. 5, 488
497. Available from: https://doi.org/10.1080/17458081003649648. Parisi, C., Vigani, M., Rodrı´guez-Cerezo, E., 2015. Agricultural nanotechnologies: what are the current possibilities? Nano Today 10, 124
127. Available from: https://doi.org/10.1016/j.nantod.2014.09.009. Park, H., Ko, E., Ahn, Y.J., 2014. Small heat shock proteins can confer tolerance to nanomaterial-induced toxicity. HortScience 49, 1116
1121. Park, D.Y., Naing, A.H., Ai, T.N., et al., 2017. Synergistic effect of nano-sliver with sucrose on extending vase life of the Carnation cv. Edun. Front. Plant Sci. 8. Available from: https://doi.org/10.3389/fpls.2017.01601. Pe´rez-de-Luque, A., 2017. Interaction of nanomaterials with plants: what do we need for real applications in agriculture? Front. Environ. Sci. 5. Available from: https://doi.org/10.3389/fenvs.2017.00012. Pinedo-Guerrero, Z.H., Herna´ndez-Fuentes, A.D., Ortega-Ortiz, H., et al., 2017. Cu nanoparticles in hydrogels of chitosan-PVA affects the characteristics of post-harvest and bioactive compounds of Jalapen˜o pepper. Molecules 22, 926. Available from: https://doi.org/10.3390/molecules22060926. Pokhrel, L.R., Dubey, B., 2013. Evaluation of developmental responses of two crop plants exposed to silver and zinc oxide nanoparticles. Sci. Total Environ. 452
453, 321
332. Available from: https://doi.org/10.1016/j. scitotenv.2013.02.059. Pradhan, S., Patra, P., Mitra, S., et al., 2015. Copper nanoparticle (CuNP) nanochain arrays with a reduced toxicity response: a biophysical and biochemical outlook on Vigna radiata. J. Agric. Food Chem. 63, 2606
2617. Available from: https://doi.org/10.1021/jf504614w. Qados, A., 2015. Mechanism of nanosilicon-mediated alleviation of salinity stress in faba bean (Vicia faba L.) plants. Am. J. Exp. Agric. 7, 78
95. Available from: https://doi.org/10.9734/AJEA/2015/15110. Qados, A., Moftah, A., 2015. Influence of silicon and nano-silicon on germination, growth and yield of faba bean (Vicia faba L.) under salt stress conditions. Am. J. Exp. Agric. 5, 509
524. Available from: https://doi.org/ 10.9734/AJEA/2015/14109. Qi, M., Liu, Y., Li, T., 2013. Nano-TiO2 improve the photosynthesis of tomato leaves under mild heat stress. Biol. Trace Elem. Res. 156, 323
328. Available from: https://doi.org/10.1007/s12011-013-9833-2. Qu, X., Alvarez, P.J.J., Li, Q., 2013. Applications of nanotechnology in water and wastewater treatment. Water Res. 47, 3931
3946. Available from: https://doi.org/10.1016/j.watres.2012.09.058. Rafique, R., Zahra, Z., Virk, N., et al., 2018. Dose-dependent physiological responses of Triticum aestivum L. to soil applied TiO2 nanoparticles: alterations in chlorophyll content, H2O2 production, and genotoxicity. Agric. Ecosyst. Environ. 255, 95
101. Available from: https://doi.org/10.1016/j.agee.2017.12.010. Rai, A.N., Penna, S., 2013. Molecular evolution of plant P5CS gene involved in proline biosynthesis. Mol. Biol. Rep. 40, 6429
6435. Available from: https://doi.org/10.1007/s11033-013-2757-2.

Plant Life under Changing Environment

References

319

Rajeshwari, A., Kavitha, S., Alex, S.A., et al., 2015. Cytotoxicity of aluminum oxide nanoparticles on Allium cepa root tip—effects of oxidative stress generation and biouptake. Environ. Sci. Pollut. Res. 22, 11057
11066. Available from: https://doi.org/10.1007/s11356-015-4355-4. Rajiv, P., Vanathi, P., 2018. Effect of Parthenium based vermicompost and zinc oxide nanoparticles on growth and yield of Arachis hypogaea L. in zinc deficient soil. Biocatal. Agric. Biotechnol. 13, 251
257. Available from: https://doi.org/10.1016/j.bcab.2018.01.006. Rajput, V.D., Minkina, T., Suskova, S., et al., 2017. Effects of copper nanoparticles (CuO NPs) on crop plants: a mini review. Bionanoscience 1
7. Available from: https://doi.org/10.1007/s12668-017-0466-3. Raliya, R., Nair, R., Chavalmane, S., et al., 2015. Mechanistic evaluation of translocation and physiological impact of titanium dioxide and zinc oxide nanoparticles on the tomato (Solanum lycopersicum L.) plant. Metallomics 7, 1584
1594. Available from: https://doi.org/10.1039/C5MT00168D. Raliya, R., Tarafdar, J.C., Biswas, P., 2016. Enhancing the mobilization of native phosphorus in the mung bean rhizosphere using ZnO nanoparticles synthesized by soil fungi. J. Agric. Food Chem. 64, 3111
3118. Available from: https://doi.org/10.1021/acs.jafc.5b05224. Ramapuram, N., Sumathi, V., Prasad TNVK, V., et al., 2018. Unprecedented synergistic effects of nanoscale nutrients on growth, productivity of sweet sorghum [Sorghum bicolor (L.) Moench], and nutrient biofortification. J. Agric. Food Chem. 66, 1075
1084. Available from: https://doi.org/10.1021/acs.jafc.7b04467. Reddy, P.V.L., Hernandez-Viezcas, J.A., Peralta-Videa, J.R., Gardea-Torresdey, J.L., 2016. Lessons learned: are engineered nanomaterials toxic to terrestrial plants? Sci. Total Environ. 568, 470
479. Available from: https:// doi.org/10.1016/j.scitotenv.2016.06.042. Rezvani, N., Sorooshzadeh, A., Farhadi, N., 2012. Effect of nano-silver on growth of saffron in flooding stress. World Acad. Sci. Eng. Technol. 6, 517
522. Rico, C.M., Lee, S.C., Rubenecia, R., et al., 2014. Cerium oxide nanoparticles impact yield and modify nutritional parameters in wheat (Triticum aestivum L.). J. Agric. Food Chem. 62, 9669
9675. Available from: https://doi. org/10.1021/jf503526r. Rico, C.M., Barrios, A.C., Tan, W., et al., 2015. Physiological and biochemical response of soil-grown barley (Hordeum vulgare L.) to cerium oxide nanoparticles. Environ. Sci. Pollut. Res. 22, 10551
10558. Available from: https://doi.org/10.1007/s11356-015-4243-y. Rizwan, M., Ali, S., Qayyum, M.F., et al., 2017. Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review. J. Hazard. Mater. 322, 2
16. Available from: https://doi.org/10.1016/j.jhazmat.2016.05.061. Roohizadeh, G., Majd, A., Arbabian, S., 2015. The effect of sodium silicate and silica nanoparticles on seed germination and growth in the Vicia faba L. Trop. Plant Res. 2, 85
89. Rossi, L., Francini, A., Minnocci, A., Sebastiani, L., 2015. Salt stress modifies apoplastic barriers in olive (Olea europaea L.): a comparison between a salt-tolerant and a salt-sensitive cultivar. Sci. Hortic. (Amsterdam) 192, 38
46. Available from: https://doi.org/10.1016/j.scienta.2015.05.023. Rossi, L., Zhang, W., Lombardini, L., Ma, X., 2016. The impact of cerium oxide nanoparticles on the salt stress responses of Brassica napus L. Environ. Pollut. 219, 28
36. Available from: https://doi.org/10.1016/j. envpol.2016.09.060. Rossi, L., Zhang, W., Ma, X., 2017. Cerium oxide nanoparticles alter the salt stress tolerance of Brassica napus L. by modifying the formation of root apoplastic barriers. Environ. Pollut. 229, 132
138. Available from: https:// doi.org/10.1016/j.envpol.2017.05.083. Ruangthep, P., Samart, S., Chutipaijit, S., 2018. ZnO nanoparticles affect differently the morphological and physiological responses of Riceberry plants (Oryza sativa L.). SNRU J. Sci. Technol. 10, 75
81. Ruttkay-Nedecky, B., Krystofova, O., Nejdl, L., Adam, V., 2017. Nanoparticles based on essential metals and their phytotoxicity. J. Nanobiotechnol. 15, 33. Available from: https://doi.org/10.1186/s12951-017-0268-3. Sabaghnia, N., Janmohammadi, M., 2015. Effect of nano-silicon particles application on salinity tolerance in early growth of some lentil genotypes. Ann. UMCS, Biol. 69, 39
55. Salata, O., 2004. Applications of nanoparticles in biology and medicine. J. Nanobiotechnol. 6, 1
6. Available from: https://doi.org/10.1186/1477-3155-2-12. Samadi, N., Yahyaabadi, S., Rezayatmand, Z., 2015. Stress effects of TiO2 and NP-TiO2 on catalase enzyme and some physiological characteristics of Melissa officinalis L. Eur. J. Med. Plants 9, 1
11. Available from: https:// doi.org/10.9734/EJMP/2015/18055.

Plant Life under Changing Environment

320

13. Nanoparticles in plants: morphophysiological, biochemical, and molecular responses

Sato, K., Ozaki, N., Nakanishi, K., et al., 2017. Effects of nanostructured biosilica on rice plant mechanics. RSC Adv. 7, 13065
13071. Available from: https://doi.org/10.1039/C6RA27317C. Sedghi, M., Hadi, M., Toluie, S., 2013. Effect of nano zinc oxide on the germination parameters of soybean seeds under drought stress. Ann. West Univ. Timi¸soara, Ser. Biol. 16, 73
78. Sekhon, S.B., 2014. Nanotechnology in agri-food production: an overview. Nanotechnol. Sci. Appl. 7, 31
53. Available from: https://doi.org/10.2147/NSA.S39406. Servin, A.D., White, J.C., 2016. Nanotechnology in agriculture: next steps for understanding engineered nanoparticle exposure and risk. NanoImpact 1, 9
12. Available from: https://doi.org/10.1016/j.impact.2015. 12.002. Shankramma, K., Yallappa, S., Shivanna, M.B., Manjanna, J., 2016. Fe2O3 magnetic nanoparticles to enhance S. lycopersicum (tomato) plant growth and their biomineralization. Appl. Nanosci. 6, 983
990. Available from: https://doi.org/10.1007/s13204-015-0510-y. Shi, J., Peng, C., Yang, Y., Yang, J., Zhang, H., Yuan, X., et al., 2014. Phytotoxicity and accumulation of copper oxide nanoparticles to the Cu-tolerant plant Elsholtzia splendens. Nanotoxicology 8, 179
188. Available from: https://doi.org/10.3109/17435390.2013.766768. Shobha, G., Moses, V., Ananda, S., 2014. Biological synthesis of copper nanoparticles and its impact—a review. Int. J. Pharm. Sci. Invent. 3, 28
38. Siddiqui, M.H., Al-Whaibi, M.H., Faisal, M., Al Sahli, A.A., 2014. Nano-silicon dioxide mitigates the adverse effects of salt stress on Cucurbita pepo L. Environ. Toxicol. Chem. 33, 2429
2437. Available from: https://doi. org/10.1002/etc.2697. Singh, A., Singh, N.B., Hussain, I., Singh, H., 2017. Effect of biologically synthesized copper oxide nanoparticles on metabolism and antioxidant activity to the crop plants Solanum lycopersicum and Brassica oleracea var. botrytis. J. Biotechnol. 262, 11
27. Available from: https://doi.org/10.1016/j.jbiotec.2017.09.016. Singh, A., Prasad, S.M., Singh, S., 2018. Impact of nano ZnO on metabolic attributes and fluorescence kinetics of rice seedlings. Environ. Nanotechnol. Monit. Manage. 9, 42
49. Available from: https://doi.org/10.1016/j. enmm.2017.11.006. Sinha, A.K., Jaggi, M., Raghuram, B., Tuteja, N., 2011. Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal. Behav. 6, 196
203. Available from: https://doi.org/10.4161/psb.6.2.14701. Soares, C., Branco-Neves, S., de Sousa, A., et al., 2018. SiO2 nanomaterial as a tool to improve Hordeum vulgare L. tolerance to nano-NiO stress. Sci. Total Environ. 622
623, 517
525. Available from: https://doi.org/10.1016/j. scitotenv.2017.12.002. Soliman, A.S., El-feky, S.A., Darwish, E., 2015. Alleviation of salt stress on Moringa peregrina using foliar application of nanofertilizers. J. Hortic. For. 7, 36
47. Available from: https://doi.org/10.5897/JHF2014.0379. Soltani, M., Kafi, M., Nezami, A., Taghiyari, H.R., 2017. Effects of silicon application at nano and micro scales on the growth and nutrient uptake of potato minitubers (Solanum tuberosum var. Agria) in greenhouse conditions. Bionanoscience . Available from: https://doi.org/10.1007/s12668-017-0467-2. Sosan, A., Svistunenko, D., Straltsova, D., et al., 2016. Engineered silver nanoparticles are sensed at the plasma membrane and dramatically modify the physiology of Arabidopsis thaliana plants. Plant J. 85, 245
257. Available from: https://doi.org/10.1111/tpj.13105. Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G., 2012. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35, 259
270. Available from: https://doi.org/10.1111/j.13653040.2011.02336.x. Syu, Y.Y., Hung, J.H., Chen, J.C., Chuang, H.W., 2014. Impacts of size and shape of silver nanoparticles on Arabidopsis plant growth and gene expression. Plant Physiol. Biochem. 83, 57
64. Available from: https://doi. org/10.1016/j.plaphy.2014.07.010. ´ ´ Szymanska, R., Kołodziej, K., Slesak, I., et al., 2016. Titanium dioxide nanoparticles (100
1000 mg/l) can affect vitamin E response in Arabidopsis thaliana. Environ. Pollut. 213, 957
965. Available from: https://doi.org/ 10.1016/j.envpol.2016.03.026. Tang, Y., He, R., Zhao, J., et al., 2016. Oxidative stress-induced toxicity of CuO nanoparticles and related toxicogenomic responses in Arabidopsis thaliana. Environ. Pollut. 212, 605
614. Available from: https://doi.org/ 10.1016/j.envpol.2016.03.019. Tantawy, A.S., Salama, Y., El-Nemr, M.A., Abdel-Mawgoud, A., 2015. Nano silicon application improves salinity tolerance of sweet pepper plants. Int. J. ChemTech Res. 8, 11
17.

Plant Life under Changing Environment

References

321

Thiruvengadam, M., Gurunathan, S., Chung, I.-M., 2015. Physiological, metabolic, and transcriptional effects of biologically-synthesized silver nanoparticles in turnip (Brassica rapa ssp. rapa L.). Protoplasma 252, 1031
1046. Available from: https://doi.org/10.1007/s00709-014-0738-5. Thiruvengadam, M., Rajakumar, G., Chung, I.-M., 2018. Nanotechnology: current uses and future applications in the food industry. 3 Biotech. 8, 74. Available from: https://doi.org/10.1007/s13205-018-1104-7. Thuesombat, P., Hannongbua, S., Ekgasit, S., Chadchawan, S., 2016. Effects of silver nanoparticles on hydrogen peroxide generation and antioxidant enzyme responses in rice. J. Nanosci. Nanotechnol. 16, 8030
8043. Available from: https://doi.org/10.1166/jnn.2016.12754. Tripathi, D.K., Singh, V.P., Prasad, S.M., et al., 2015. Silicon nanoparticles (SiNp) alleviate chromium (VI) phytotoxicity in Pisum sativum (L.) seedlings. Plant Physiol. Biochem. 96, 189
198. Available from: https://doi.org/ 10.1016/j.plaphy.2015.07.026. Tripathi, D.K., Singh, S., Singh, V.P., et al., 2016. Silicon nanoparticles more efficiently alleviate arsenate toxicity than silicon in maize cultiver and hybrid differing in arsenate tolerance. Front. Environ. Sci. 4. Available from: https://doi.org/10.3389/fenvs.2016.00046. Tripathi, A., Liu, S., Singh, P.K., et al., 2017a. Differential phytotoxic responses of silver nitrate (AgNO3) and silver nanoparticle (AgNps) in Cucumis sativus L. Plant Gene 11, 255
264. Available from: https://doi.org/ 10.1016/j.plgene.2017.07.005. Tripathi, D.K., Shweta, Singh, S., et al., 2017b. An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiol. Biochem. 110, 2
12. Available from: https://doi. org/10.1016/j.plaphy.2016.07.030. Tripathi, D.K., Singh, S., Singh, V.P., et al., 2017c. Silicon nanoparticles more effectively alleviated UV-B stress than silicon in wheat (Triticum aestivum) seedlings. Plant Physiol. Biochem. 110, 70
81. Available from: https://doi.org/10.1016/j.plaphy.2016.06.026. Tumburu, L., Andersen, C.P., Rygiewicz, P.T., Reichman, J.R., 2017. Molecular and physiological responses to titanium dioxide and cerium oxide nanoparticles in Arabidopsis. Environ. Toxicol. Chem. 36, 71
82. Available from: https://doi.org/10.1002/etc.3500. Tung, H.T., Nam, N.B., Huy, N.P., et al., 2018. A system for large scale production of chrysanthemum using microponics with the supplement of silver nanoparticles under light-emitting diodes. Sci. Hortic. (Amsterdam) 232, 153
161. Available from: https://doi.org/10.1016/j.scienta.2017.12.063. Upadhyaya, H., Begum, L., Dey, B., et al., 2017. Impact of calcium phosphate nanoparticles on rice plant. J. Plant Sci. Phytopathol. 1, 001
010. Available from: https://doi.org/10.29328/journal.jpsp.1001001. Vaculı´k, M., Konlechner, C., Langer, I., et al., 2012. Root anatomy and element distribution vary between two Salix caprea isolates with different Cd accumulation capacities. Environ. Pollut. 163, 117
126. Available from: https://doi.org/10.1016/j.envpol.2011.12.031. Vannini, C., Domingo, G., Onelli, E., et al., 2013. Morphological and proteomic responses of Eruca sativa exposed to silver nanoparticles or silver nitrate. PLoS One 8, e68752. Available from: https://doi.org/10.1371/journal. pone.0068752. Veˇceˇrova´, K., Veˇceˇra, Z., Doˇcekal, B., et al., 2016. Changes of primary and secondary metabolites in barley plants exposed to CdO nanoparticles. Environ. Pollut. 218, 207
218. Available from: https://doi.org/10.1016/j. envpol.2016.05.013. Vishwakarma, K., Upadhyay, N., Kumar, N., et al., 2017. Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant Sci. 8. Available from: https://doi. org/10.3389/fpls.2017.00161. Wang, Q., Ma, X., Zhang, W., et al., 2012. The impact of cerium oxide nanoparticles on tomato (Solanum lycopersicum L.) and its implications for food safety. Metallomics 4, 1105. Available from: https://doi.org/10.1039/c2mt20149f. Wang, P., Lombi, E., Zhao, F.-J., Kopittke, P.M., 2016a. Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci. 21, 699
712. Available from: https://doi.org/10.1016/j.tplants.2016.04.005. Wang, Y., Hu, J., Dai, Z., et al., 2016b. In vitro assessment of physiological changes of watermelon (Citrullus lanatus) upon iron oxide nanoparticles exposure. Plant Physiol. Biochem. 108, 353
360. Available from: https:// doi.org/10.1016/j.plaphy.2016.08.003. Wang, Z., Xu, L., Zhao, J., et al., 2016c. CuO nanoparticle interaction with Arabidopsis thaliana: toxicity, parentprogeny transfer, and gene expression. Environ. Sci. Technol. 50, 6008
6016. Available from: https://doi.org/ 10.1021/acs.est.6b01017.

Plant Life under Changing Environment

322

13. Nanoparticles in plants: morphophysiological, biochemical, and molecular responses

Wang, Y., Chen, R., Hao, Y., et al., 2017. Transcriptome analysis reveals differentially expressed genes (DEGs) related to lettuce (Lactuca sativa) treated by TiO2/ZnO nanoparticles. Plant Growth Regul. 83, 13
25. Available from: https://doi.org/10.1007/s10725-017-0280-5. Wu, H., Tito, N., Giraldo, J.P., 2017. Anionic cerium oxide nanoparticles protect plant photosynthesis from abiotic stress by scavenging reactive oxygen species. ACS Nano 11, 11283
11297. Available from: https://doi.org/ 10.1021/acsnano.7b05723. Yang, F., Hong, F., You, W., et al., 2006. Influences of nano anatase TiO2 on nitrogen metabolism of growing spinach. Biol. Trace Elem. Res. 110, 179
190. Yang, K.Y., Doxey, S., McLean, J.E., et al., 2017. Remodeling of root morphology by CuO and ZnO nanoparticles: effects on drought tolerance for plants colonized by a beneficial pseudomonad. Botany 1
12. Available from: https://doi.org/10.1139/cjb-2017-0124. Yanık, F., Vardar, F., 2015. Toxic effects of aluminum oxide (Al2O3) nanoparticles on root growth and development in Triticum aestivum. Water Air Soil Pollut. 226, 296. Available from: https://doi.org/10.1007/s11270-0152566-4. Yasmeen, F., Raja, N.I., Razzaq, A., Komatsu, S., 2016. Gel-free/label-free proteomic analysis of wheat shoot in stress tolerant varieties under iron nanoparticles exposure. Biochim. Biophys. Acta, Proteins Proteomics 1864, 1586
1598. Available from: https://doi.org/10.1016/j.bbapap.2016.08.009. Yasmeen, F., Raja, N.I., Razzaq, A., Komatsu, S., 2017. Proteomic and physiological analyses of wheat seeds exposed to copper and iron nanoparticles. Biochim. Biophys. Acta, Proteins Proteomics 1865, 28
42. Available from: https://doi.org/10.1016/j.bbapap.2016.10.001. Yin, H., Casey, P.S., McCall, M.J., Fenech, M., 2010. Effects of surface chemistry on cytotoxicity, genotoxicity, and the generation of reactive oxygen species induced by ZnO nanoparticles. Langmuir 26, 15399
15408. Available from: https://doi.org/10.1021/la101033n. Yoshida, T., Fujita, Y., Maruyama, K., et al., 2015. Four A rabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ. 38, 35
49. Available from: https://doi.org/10.1111/pce.12351. Yuan, J., Chen, Y., Li, H., et al., 2018. New insights into the cellular responses to iron nanoparticles in Capsicum annuum. Sci. Rep. 8, 3228. Available from: https://doi.org/10.1038/s41598-017-18055-w. Yunus, I.S., Harwin, A.K., Kurniawan, A., et al., 2012. Nanotechnologies in water and air pollution treatment. Environ. Technol. Rev. 1, 136
148. Available from: https://doi.org/10.1080/21622515.2012.733966. Zahra, Z., Arshad, M., Rafique, R., et al., 2015. Metallic nanoparticle (TiO2 and Fe3O4) application modifies rhizosphere phosphorus availability and uptake by Lactuca sativa. J. Agric. Food Chem. 63, 6876
6882. Available from: https://doi.org/10.1021/acs.jafc.5b01611. Zhao, L., Peng, B., Hernandez-Viezcas, J.A., et al., 2012. Stress response and tolerance of Zea mays to CeO2 nanoparticles: cross talk among H2O2, heat shock protein, and lipid peroxidation. ACS Nano 6, 9615
9622. Available from: https://doi.org/10.1021/nn302975u. Zhao, J., Ren, W., Dai, Y., et al., 2017a. Uptake, distribution, and transformation of CuO NPs in a floating plant Eichhornia crassipes and related stomatal responses. Environ. Sci. Technol. 51, 7686
7695. Available from: https://doi.org/10.1021/acs.est.7b01602. Zhao, L., Hu, Q., Huang, Y., et al., 2017b. Activation of antioxidant and detoxification gene expression in cucumber plants exposed to a Cu(OH)2 nanopesticide. Environ. Sci. Nano 4, 1761. Available from: https://doi.org/ 10.1039/C7EN90033C. Zhao, D., Cheng, M., Tang, W., et al., 2018. Nano-silver modifies the vase life of cut herbaceous peony (Paeonia lactiflora Pall.) flowers. Protoplasma. Available from: https://doi.org/10.1007/s00709-018-1209-1. Zheng, L., Hong, F., Lu, S., Liu, C., 2005. Effect of nano-TiO2 on strength of naturally aged seeds and growth of spinach. Biol. Trace Elem. Res. 104, 083
092. Available from: https://doi.org/10.1385/BTER:104:1:083.

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C H A P T E R

14 Regulations of reactive oxygen species in plants abiotic stress: an integrated overview Shiliang Liu and Rongjie Yang College of Landscape Architecture, Sichuan Agricultural University, Chengdu, P.R. China

14.1 Introduction Reactive oxygen species (ROS) is considered as an unwelcome partner in Earth’s aerobic organisms, since oxygen molecules (O2) were introduced from the atmosphere by O2evolved photosynthetic organisms about 3 billion years ago (Kovtun et al., 2000; Jaspers and Kangasja¨rvi, 2010; Dickinson and Chang, 2011; Das and Roychoudhury, 2014; Liu et al., 2015a,b,c,d; Xia et al., 2015; Mittler, 2011, 2017). Unlike O2, various reactive oxygen derivatives [e.g., singlet oxygen (1O2), hydrogen peroxide (H2O2), and superoxide radical (O
2 2 )] under unfavorable conditions have high toxicity, thus causing oxidative stress in organism cells (Table 14.1; Halliwell and Gutteridge, 1989, 2007; Laloi et al., 2004; Van Breusegem et al., 2008; Murphy et al., 2011; Liu et al., 2015a,b,c,d; Gilroy et al., 2016). In general, abiotic stress emerges when the environment deviates from optimal conditions that interfere with cellular function, which is also defined as the stress of any factor other than direct interaction with another organism (Gill and Tuteja, 2010; Murphy et al., 2011; Choudhury et al., 2013). In addition, the delicate balance between the generation and removal of ROS is interfered by different types of stressors (Møller et al., 2007; Baxter et al., 2014), among which the most frequently mentioned ones are drought, salinity, heavy metals, extreme temperature, excessive light, and ultraviolet (UV) radiation, as well as xenobiotic, ozone, sulfur dioxide (SO2), elevated CO2 (carbon dioxide), and nutrient deficiencies (Mittler, 2006; Van Breusegem et al., 2008; Cramer et al., 2011; Wrzaczek et al., 2013; Zhu, 2016). In higher plants, those abiotic stresses usually stimulate ROS formation (a common event regardless of plant species), causing a variety of physiological variations (Foyer and Noctor, 2005a,b; Gratao et al., 2005; Choudhury et al., 2013). However, it is

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00017-5

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© 2020 Elsevier Inc. All rights reserved.

TABLE 14.1 The properties (half-life time and migration distance), reactivity (mode of action), formation (typical reaction formula), and scavenging (typical scavenging systems) of the reactive oxygen species (ROS) family and itsvarious targets in plant cells. Halflife time (t1/2)

Migration distance

Superoxide radical (O
2 2 )

24 μs

1

Name

MoA

30 nm

Mitochondria, apoplast (RBOHs), chloroplasts, membranes, peroxisomes, endoplasmic reticulum and cell walls

Reacts with the double bond, for example, ironsulfur proteins

1 2 4 μs 30 nm

Mitochondria, chloroplasts, and membranes

Oxidizes proteins, G residues of DNA and PUFAs

H2O2

.1 ms

.1 μs

Mitochondria, chloroplasts, membranes, peroxisomes, apoplast, and cell walls

Reacts with DNA and proteins, for example, reacting with oxidizes/heme proteins and forming OHd via O
2 2 by attacking cysteine and methionine residues

Hydroxyl radical (OHd)

1 μs

1 nm

Chloroplasts, mitochondria, membranes, and cell walls

Alkoxy radicals (ROd)

?

1 nm

Plasma membrane, and peroxydation

Reacts with protein, lipid and carbohydrate (PUFA)

1. RO• 1 HO2-RO2• 1 HO 2. RO• 1 R0 O2-RO2• 1 R0 O

Flavonoids, nitrone/nitroso, phenolics, trolox, etc.

Peroxy radicals (ROOd)

?

1 nm

Plasma membrane, and peroxydation

Reacts with protein, lipid and carbohydrate (PUFA)

1. Initiation step Initiator -R
2. Propagation step R
1 O2-ROO
ROO
1 RH-ROOH 1 R
3. Termination step ROO
1 ROO
-nonradical products

Flavonoids, phenolics, AsAGSH system, etc.

O2

Targets of ROS Damages

Disruptive behavior

Reaction formula

Scavenging systems

Site of generation

31 1 21 1. O
2 SOD, GSH, 2 1 Fe - O2 1 Fe 1 2. O
2 1 2H -O 1 H O flavonoids, etc. 2 2 2 2 3. Fe21 1 H2O2-Fe31 1 OH2 1 OH• (Fenton reaction)

1. Chl-3Chl 2. 3Chl 1 3O2 - Chl 1 1O2

1 1. 2O
2 2 1 2H -H2O2 1 O2

2 • Extremely reactive with all biomolecules, 1. H2O2 1 O
2 2 -OH 1 O2 1 OH for example, lipids, proteins DNA, and RNA

Reaction formula

Carotenoids, proline, α-tocopherol, GR, GSH, etc. Catalase, ascorbic acid, flavonoids APX, GPX, PER, PRX, GSH, etc. Flavonoids, proline, sugars, GR, GSH, etc.

Targets of ROS Damages

Disruptive behavior

Lipids

Lipid Enhance membrane fluidity and permeability and breaking of lipid chains peroxidation

Proteins

Protein oxidation

Modified amino acids, breakage of the peptide chain, increased proteolytic degradation, and inactivation of enzyme

DNA

DNA damage

Breaking of stand, depurination and depyrimidination, mutation of bases, and protein DNA cross-links

Reaction formula 1. Initiation step RH 1 OH
-H2O 1 R
(lipid alkyl radical) 2. Propagation step R
1 O2-ROO
(lipid peroxy radical) ROO
1 RH-ROOH 1 R
ROOH-RO
(epoxides, hydroperoxides, glycol, and aldehydes) 3. Termination step R
1 R
-R 1 R (fatty-acid dimer) R
1 ROO
-ROOR (peroxide-bridged dimer) ROO
1 ROO
-O2 1 ROOR (peroxide-bridged dimer)

1 O2, Singlet oxygen; APX, ascorbate peroxidase; CAT, catalase; Chl, chloroplast; DNA, deoxyribonucleic acid; Fe, iron; GPX, glutathione peroxidase; GSH, reduced glutathione. GR, glutathione reductase; H2O2, hydrogen peroxide; MoA, mode of action; O2, oxygen; PER, peroxidase; PRX, peroxiredoxin; PUFAs, polyunsaturated fatty acids; RBOHs, respiratory burst oxidase homologs; SOD, superoxide dismutase; RNA, ribonucleic acid. Referred/modified by Ko¨nig, J., Muthuramalingam, M., Dietz, K.J., 2012. Mechanisms and dynamics in the thiol/disulfide redox regulatory network: transmitters, sensors and targets. Curr. Opin. Plant Biol. 15, 261268; Foyer, C.H., Noctor, G., 2013. Redox signaling in plants. Antioxid. Redox Signal. 18, 20872090; Vaahtera, L., Brosche´, M., Wrzaczek, M., Kangasja¨rvi, J., 2014. Specificity in ROS signaling and transcript signatures. Antioxid. Redox Signal. 21, 14221441; Mignolet-Spruyt, L., Xu, E., Ida¨nheimo, N., Hoeberichts, F.A., Mu¨hlenbock, P., Brosche´, M., et al., 2016. Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J. Exp. Bot. 67, 38313844; Mittler, R., 2017. ROS are good. Trends Plant Sci. 22, 1119.

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14. Regulations of reactive oxygen species in plants abiotic stress: an integrated overview

worth noting whether the role of ROS in cells functions as protection, destruction, or signal transduction, which mainly relies on the delicate equilibrium between the generation and clearance of ROS at appropriate locations and time points (Foyer and Noctor, 2013; Laurindo et al., 2014; Zhu, 2016). Definitely, a good equilibrium exists between the signaling of ROS generation, the reactivity of ROS diffusion, the baseline of ROS metabolism, and the perception of ROS signaling in different cells’ compartments of plants throughout the evolution process (ROS network; Mittler et al., 2004, 2017). For example, ROS induced by stress could be neutralized by plasma membrane-bound NADPH oxidases [i.e., respiratory burst oxidase homolog, rubidium hydroxides (RBOHs); and termed NADPHdependent-oxidases (NOXs) in plants] and enzymatic antioxidant systems consisting numerous scavengers (Table 14.2) such as catalase, peroxidase (POD), and superoxide dismutase (SOD), and nonenzymatic compounds, such as ascorbate, glutathione (GSH), and flavonoids (Dickinson and Chang, 2011; Ko¨nig et al., 2012; Vaahtera et al., 2014). Under abiotic stress, redox metabolism and its corresponding signaling are often considered as a key mechanism in plants (Mittler et al., 2004; Murphy et al., 2011; Zhu, 2016). During evolution, plants have developed a unique mechanism for active controlling of ROS overproduction and for effectively using it as a signaling molecule (Ko¨nig et al., 2012; Munne´Bosch et al., 2013). To date, many signal-transduction pathways that regulated by ROS have been reported (Foyer and Noctor, 2013; Mittler, 2017). However, the recognition of ROS-mediated signaling is discontinuous, the specificities of ROS-signal sensing and conduction remains unresolved. Some previous publications (e.g., Møller et al., 2007; Mittler et al., 2011; Tripathy and Oelmu¨ller, 2012; Choudhury et al., 2013; Wrzaczek et al., 2013) can be used as reference in the reviews of ROS signaling. However, few current reviews are reported regarding the relationship between abiotic stress and ROS regulation. Therefore in this review, we focused on the integration of ROS-regulated sites, the involvement of antioxidants, and the regulatory role of ROS signalings in plants under abiotic stress over the past few years.

14.2 Reactive oxygen species regulation in plant organelles during abiotic stress ROS, a toxic by-product of toxic metabolites (Jaspers and Kangasja¨rvi, 2010; Rodrı´guezSerrano et al., 2016), is mainly formed in chloroplasts, mitochondria, apoplasts, peroxisomes, and other sites during abiotic stress in higher plants (Table 14.1). The formation is also included in any other cellular compartment that contains proteins or molecules with sufficiently high redox potentials to stimulate/provide electrons to atmospheric O2 (Vaahtera et al., 2014; Takagi et al., 2016). Under abiotic stress conditions, variation behaviors including the increased rate of ROS generation and together with the decreased capacity of antioxidant scavenging will result in the significant accumulation of ROS in plants (Jaspers and Kangasja¨rvi, 2010). Currently, many studies have well determined the toxic effects of ROS on cellular components and the signaling function of ROS on cellular mechanisms (see Fig. 14.1, e.g., Dickinson and Chang, 2011; Foyer and Noctor, 2009, 2013; Mignolet-Spruyt et al., 2016; Mittler, 2017).

Plant Life under Changing Environment

TABLE 14.2 Major enzymatic and nonenzymatic antioxidants and their function and subcellular localization in plants under abiotic stress. Enzymatic antioxidants

Enzyme code

Reactions catalyzed

Subcellular location

APX

EC 1.11.1.11

H2O2 1 AA-2H2O 1 DHA

Chloroplast, cytoplasm, peroxisomes, and mitochondria

CAT

EC 1.11.1.6

2H2O2-2H2O 1 O2

Peroxisome and mitochondria

DHAR

EC 1.8.5.1

DHA 1 2GSH-AA 1 GSSG

Chloroplast, cytoplasm, and mitochondria

GPOX

EC 1.11.1.7

H2O2 1 GSH-H2O 1 GSSG

Mitochondria, cytoplasm, chloroplast, and endoplasmic reticulum

Glutathione peroxidase (GPX)

EC 1.11.1.12

2GSH 1 PUFAOOH-GSSG 1 PUFA 1 2H2O

Chloroplast, cytoplasm, and mitochondria

GR

EC 1.6.4.2

GSSG 1 NAD(P)H-2GSH 1 NAD(P)1

Chloroplast, cytoplasm, and mitochondria

GST

EC 2.5.1.18

RX 1 GSH-HX 1 R-S-GSH

Chloroplast, cytoplasm, peroxisome, mitochondria

MDHAR

EC 1.6.5.4

MDHA 1 NAD(P)H-AA 1 NAD(P)1

Chloroplast, cytoplasm, and mitochondria

PHGPX

EC 1.11.1.9

2GSH 1 PUFAOOH(H2O)-GSSG 1 2H2O

Chloroplast, cytoplasm, and mitochondria

PPO

EC 1.10.3.1

Monophenol/Diphenol 1 O2 1 PPO-dephenol/ quinone 1 H2O

Cytoplasm, chloroplast, peroxisomes, and mitochondria

SOD

EC 1.15.1.1

1
2 O
2 2 1 O2 1 2H -2H2O2 1 O2

Chloroplast, cytoplasm, peroxisomes, and mitochondria

Nonenzymatic antioxidants

Function

Subcellular location

ascorbic acid (AsA)

Detoxifies H2O2 via action of APX

Apoplast, chloroplast, cytoplasm, mitochondria, peroxisome, and vacuole

Car

Quenches excess energy from the photosystems and light harvesting complexes

Chloroplasts and other nongreen plastids

Flavonoids

Direct scavengers of H2O2 and 1O2 and OH•

Vacuole

•

1

Free amino acids (such as arginine, histidine, and proline)

Efficient scavenger of OH and O2 and prevent damages due to lipid peroxidation

Chloroplast, cytoplasm, and mitochondria

Reduced GSH

Acts as a detoxifying cosubstrate for enzymes such as peroxidases, GR, and GST

Apoplast, chloroplast, cytoplasm, mitochondria, peroxisome, and vacuole

Tocopherols (including α, β, γ, and δ)

Guards against and detoxifies products of membrane lipid peroxidation

Mostly in membranes

APX, Ascorbate peroxidase; CAT, catalase; CAR, carotenoids; DHA, docosahexaenoic acid; DHAR, dehydroascorbate reductase; GPOX, guaiacol-type peroxidase; GR, glutathione reductase; GSSG, glutathione disulfide; GSH, glutathione; GST, glutathine S-transferases; H2O2, hydrogen peroxide; MDHA, monodehydroisosorbide; MDHAR, monodehydroascorbate reductase; NADP1, nicotinamide adenine dinucleotide phosphate; O2, oxygen; PHGPX, phospholipid-hydroperoxide glutathione peroxide; PPO, polyphenol oxidase; PUFA, polyunsaturated fatty acid; PUFA-OOH, PUFA hydroperoxide; SOD, superoxide dismutase.

Referred and modified by Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909930; Choudhury, S., Panda, P., Sahoo, L., Panda, S.K., 2013. Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav. 8, e23681. Available from: https://doi:10.4161/psb.23681; Das, K., Roychoudhury, A., 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci., 2, e53. Available from: https://doi:0.3389/fenvs.2014.00053; Malar, S., Vikram, S.S., Jc Favas, P., Perumal, V., 2016. Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud. 55, 54. Available from: https://doi:10.1186/s40529-014-0054-6; Hasanuzzaman, M., Nahar, K., Anee, T.I., Fujita, M., 2017. Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol. Mol. Biol. Plants 23, 249268; Pandey, S., Fartyal, D., Agarwal, A., Shukla, T., James, D., Kaul, T., et al., 2017. Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci. 8: 581. Available from: https://doi:10.3389/fpls.2017.00581; Liu, S.L., Yang, R.J., Tripathi, D.K., Li, X., He, W., Wu, M.X., et al., 2018. The interplay between reactive oxygen and nitrogen species contributes in the regulatory mechanism of the nitro-oxidative stress induced by cadmium in Arabidopsis. J. Hazard. Mater. 344, 10071024.

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14. Regulations of reactive oxygen species in plants abiotic stress: an integrated overview

FIGURE 14.1 Schematic illustration of the generation of ROS in different organelles and their corresponding regulatory roles within or among different organelles in plant cells. Dark-orange graphics (round box) represent different types of reactive oxygen species. The green isosceles pentagons (pentagon box) represent the action of antioxidant enzymes on ROS in plant organelles. Arrows represent the processes of metabolism or signaling between different substances. 1O2, Singlet oxygen; APX, ascorbate peroxidase; CAT, catalase; Cyt b, cytochrome b; Cyt C1, cytochrome C1 or complex III subunit 4; Cyt. aa3, cytochrome aa3; DHAR, dehydroascorbate reductase; FeS, ironsulfur; FMN, flavin mononucleotide or riboflavin-50 -phosphate; GPX, glutathione peroxidase; GR, glutathione reductase; GST, glutathine S-transferases; H2O2, hydrogen peroxide; LHCII, light-harvesting complex II; MDHAR, monodehydroascorbate reductase; NADPH, nicotinamide adenine dinucleotide phosphate; O
2 2 , superoxide radical; OH•, hydroxyl radical; P450, P600, and P700, which are derived from the spectrophotometric peak at the wavelength of the absorption maximum of the enzyme (450, 600, and 700 nm) when it is in the reduced state and complexed with carbon monoxide; RBOH, respiratory burst oxidase homolog; RO•, alkoxy radical; ROS, reactive oxygen species; ROO•, peroxy radical; SOD, superoxide dismutase; UQ, ubiquinones. Source: Modified from Bhattacharjee, S., 2012. The language of reactive oxygen species signaling in plants. J. Bot. 2012, e985298. Available from: https://doi.org/10.1155/ 2012/985298; Mittler, R., 2017. ROS are good. Trends Plant Sci. 22, 1119; Hasanuzzaman, M., Nahar, K., Anee, T.I., Fujita, M., 2017. Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol. Mol. Biol. Plants 23, 249268; Caverzan, A., Passaia, G., Rosa, S.B., Ribeiro, C.W., Lazzarotto, F., Margis-Pinheiro, M., 2012. Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genet. Mol. Biol. 35, 10111019.

14.2.1 Chloroplasts Chloroplasts, the primary site of ROS in photosynthetic tissues, produce high amounts of ROS in higher plants (Dietz et al., 2016). Especially, ROS occur in plant cells when exposed to a decrease in photosynthetic carbon fixation, which is a typical stress response under abiotic stress (Takahashi and Murata, 2008; Gilroy et al., 2016). The electron flow [e.g., electrontransport chain (ETC) and triplet chlorophyll (3Chl)] from the center of the excited photosystem (PSI and PSII) is typically directed to NADP1/NADPH. It reduced the final electron acceptor to CO2 through the Calvin cycle (Foyer and Noctor, 2009, 2013). In the case of ETC

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14.2 Reactive oxygen species regulation in plant organelles during abiotic stress

329

overload, partial electron flows are transferred from ferredoxin (FeS proteins) to O2, which is reduced to O
2 2 by the “Mehler reaction” as shown in the following equation: 2O2 1 2Fdred -2O
2 2 1 2Fdox where Fdred is the reduced ferredoxin; Fdox, endergonic reduction (ER) of ferredoxin (Wise and Naylor, 1987; Elstner, 1991; Wang et al., 2010a,b). Another common point of leakage electrons from the ETC of PSI are 2Fe2S and 4Fe4S clusters (Das and Roychoudhury, 2014). In PSII the acceptor side of ETC also provides specific electron leakage [e.g., primary and secondary receptor plastids (QA and QB)] for the production of 1O2 (Takahashi and Murata, 2008; Chen and Dickman, 2004; Gill and Tuteja, 2010). The 1O2, a by-product of photosynthesis, is unusually generated in chloroplasts PSII by the stimulated chlorophyll molecules under photoinhibition or low-light conditions as shown in the equation (Mur et al., 2008; Buchert and Forreiter, 2010; Das and Roychoudhury, 2014): 3Chl 1 3O2 -Chl 1 1 O2 As complementary, recent studies also verified that the chloroplast-produced ROS have the capability to transmit the spread of wound-induced PCD (i.e., programmed cell death) in plant tissues (Gray et al., 2002; Krieger-Liszkay et al., 2008; Gill and Tuteja, 2010). In addition, chloroplasts play a crucial regulatory role in apoptotic PCD. For instance, the light-grown cultures with antioxidant in Arabidopsis plants resulted in the upregulation of the apoptotic-like PCD, indicating the chloroplast and corresponded ROS may involve in apoptotic-like PCD (Doyle et al., 2010). Besides, Hu et al. (2008) also found that chilling stress induced ROS accumulation in cucumber plants, thus decreasing the net photosynthetic rate but increasing the resistance mechanisms including ROS scavenging antioxidants and thermal dissipation. Therefore the controlling or clearance of ROS in chloroplasts is critical to ensure continuous survival of plants exposed to abiotic stress, as confirmed in some transgenic plants and in stress-tolerant cultivars (Chen and Dickman, 2004; Das and Roychoudhury, 2014).

14.2.2 Mitochondria Mitochondria as a “power plant” is defined as the largest source of ROS production and targets in nonphotosynthetic tissues (Rasmusson et al., 2004), but their contribution to plant cells is relatively small in comparison with that of chloroplasts (Chen and Dickman, 2004; Navrot et al., 2007; Jaspers and Kangasja¨rvi, 2010). Unlike in animals, the redox state of mitochondria in plants has specific components/functions of ETC (such as photorespiration), which is a significant marker of the cellular energy status and the ROS. Previous studies confirmed that the two complexes (I and III) derived from the mitochondrial ETC are important sites for ROS (especially O
2 2 ), which is downregulated by the dismutation of SOD to H2O2 in aqueous solution as parts of the monitoring system (Noctor et al., 2006; Taylor et al., 2009). Among them, Complex I (or NADH dehydrogenase) directly depresses the oxygen/O2 to O
2 2 under optimal protein region. Due to controlled by adenosine triphosphate (ATP) hydrolysis and lack of NAD1-related substrates, however, the reverse electron flow from Complex III to I may induce an increase of ROS production in Complex I (Turrens, 2003). Murphy (2009) reported, in Complex III, ubiquinone (UQ) Plant Life under Changing Environment

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(coenzyme Q10/CoQ10) with an unstable ubisemiquinone semiradical (after donating an electron to cytochrome C1) is benefit for electron leakage to O2 thus producing the O
2 2 . Moreover, control of ROS production in plant mitochondria under abiotic stress could be achieved by an energy-dissipation system, which has been verified in mitochondria of durum wheat (Pastore et al., 2007). In the mitochondria of drought-stress-induced plants, ROS activates the specificity proteins mitoKATPs (mitochondrial ATP-sensitive potassium/K1 channels of plants) and plant-uncoupling protein or conversely dissipates the membrane potential of mitochondria (Pastore et al., 1999; Woyda-Ploszczyca and Jarmuszkiewicz, 2014), thereby reducing the likelihood of large-scale ROS production over a large range. To further explore plant mitochondria’s role in redox homeostasis, publications showed that the cytoplasmic male-sterile mutants (CMSII) may be damaged in functional Complex I but increased the respiration of NADPH dehydrogenase (cf., nonphosphorylating rotenoneinsensitive) and alternative oxidase (AOX) (cf., cyanideinsensitive), suggesting the effective in maintaining redox balance via the crosstalking and acclimation of antioxidants between the mitochondria and other organelles (Laser and Lersten, 1972; Dutilleul et al., 2003; Atkin and Macherel, 2009). Various enzymes, such as L-galactose-γ-lactone dehydrogenase (GLDH), AOX, and aconitate hydratase, are other sources of ROS production in plant mitochondria, which are committed to the direct or indirect production of ROS through multiple electron-transport pathways (Rasmusson et al., 2008; Seminario et al., 2017). For the sources of H2O2 in the mitochondria, two enzymes, APX (ascorbate POD) and Mn-SOD (manganese SOD), convert the O
2 2 into H2O2 at the rate of B1%5% of the total O2 consumption (Sharma et al., 2012). Under abiotic stress conditions, ROS production in mitochondria is driven by the tight coupling of ETC and ATP synthesis because of a decrease in electron carriers (e.g., the UQ pool; Atkin and Macherel, 2009; Boguszewska et al., 2010). Besides, two mitochondria enzymes, AOX and mitochondrial SOD (Mn-SOD), involve in the counteraction of oxidative stress. The AOX inhibit the UQ pool to slow down the production of ROS, which have been verified in the lacking or having of functional AOX in drought-stressed Arabidopsis thaliana L. plants (Ho et al., 2008). Early study also reported that the greater the difference between two tomato (Solanum lycopersicum L.) varieties (i.e., salt-tolerant and -sensitive), the higher the Mn-SOD activity under salt stress (Mittova et al., 2003).

14.2.3 Peroxisomes In plant peroxisomes, ROS (mainly H2O2 and O
2 2 ) are generated via several processes at high rates, the amount of which is mediated by the delicate equilibrium between generation and removing (Mittler et al., 2011; Corpas et al., 2017a,b; Foyer and Noctor, 2013). Two sites of the O
2 production in plant peroxisomes have been established under 2 adverse conditions: (1) the organelle matrix, where the oxidation of hypoxanthine is catalyzed by xanthine oxidase (XOD) to xanthine and further with the uric acid, and (2) the peroxisome membrane relying on NADPH, where a small ETC including the cytochrome b and flavoprotein NADH produces O
2 2 in peroxisome (Del Rı´o et al., 2002; Nyathi and Baker, 2006; Oikawa et al., 2015; Duong et al., 2017). For the generation and metabolism of H2O2 in peroxisomes, as one of the oxidases, the photorespiratory glycolate oxidases can effectively restrain gas exchange accompanied by the closure of stomata during abiotic Plant Life under Changing Environment

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stresses, resulting in the reduction of the availability of CO2 for RUBISCO and the elevation of photorespiration and H2O2 production (Hackenberg et al., 2011; Das and Roychoudhury, 2014; Ahammed et al., 2017). Several complementary metabolisms, such as the oxidation of flavin groups and fatty acids (FAs), and the disproportionation of free radicals (O
2 2 ), also contribute to ROS generation in peroxisomes. Recent studies showed that nitric-oxide (•NO) radicals or their derivative molecules can also be “switched on” in plant peroxisomes and accompanied with the complex interactive metabolism with ROS (referred by Mittler et al., 2011; Spiess and Zolman, 2013; Corpas et al., 2017a,b). These derivative molecules include S-nitrosoglutathione (GSNO), S-nitrosothiols (SNOs), peroxynitrite (ONOO2), and nitro-FAs (NO2-FA), which is often designed as reactive nitrogen species (RNS). It is well known that •NO as a free-radical gas with diatomic molecules has an important influence on signal transduction for life activities in higher plant (Mata-Pe´rez et al., 2016; Corpas and Barroso, 2017; Liu et al., 2016a, 2018). The presence of L-arginine (L-Arg)-dependent NO synthetase (NOS) has the same biochemical requirements (e.g., NADPH, calmodulin/CaM, L-Arg, flavin mononucleotide or riboflavin-50 -phosphate/FMN) as NOS-like activity in animal (Corpas et al., 2017a,b). In addition, both RNS and ROS generated in peroxisomes involve in the germination of seeds/pollens (Reichler et al., 2009), aging of leaves (Zou et al., 2015), and mediation of auxin-induced lateral root organogenesis (Schlicht et al., 2013; Corpas et al., 2017a,b). To date, no orthologs similar with the classical mammalian NOS have been found in high plants, although previous studies have reported on variations of NOS activity in animal peroxisomes (e.g., Loughran et al., 2005, 2013).

14.2.4 Apoplasts In apoplasts, four major mechanisms regulate the production of ROS during abiotic stress. First, plasma membrane NADPH oxidase RBOH protein has an important influence on the ROS production network (Foyer and Noctor, 2013), thus integrating calcium/Ca21 and ROS signaling to produce superoxide during abiotic stresses (Mittler et al., 2004, 2011; Wi et al., 2012; Baxter et al., 2014; Yamauchi et al., 2017). Studies showed that RBOHs play important roles in various signaling pathways in plants, including stomatal closure, interaction between pollen and column, and defense and adaptation to abiotic stress (Dubiella et al., 2013; Gilroy et al., 2016). Kimura et al. (2012) found that RBOHs have an important cytoplasmic FAD-/NADPH-binding domain in the C-terminal region of plants, in which six transmembrane domains correspond one to one with those in mammalian NADPH oxidase. In contrast to mammalian, plant RBOHs contain a cytoplasmic N-terminal extension consisting of two Ca-binding E-F hand motifs (Dubiella et al., 2013). Once activated, the O
2 2 is produced in the apoplasts by the action of the RBOH proteins and is spontaneously or catalytically disproportionated into H2O2 by SODs, which depend on the effects of various signal components including phospholipase Dα1, posttranslational modification of proteins or Ca21-dependent protein kinase (CDPK)/CaM-dependent protein kinase (CaMK) (Gilroy et al., 2016; Yamauchi et al., 2017). Accordingly, those H2O2 molecules are involved in the regulation of plant growth and signal transduction during cellular metabolism. Under abiotic stress, oxalate oxidase (OxOx) as a catalytic chemical reaction enzyme (i.e., oxalate 1 O2 1 2H132CO2 1 H2O2) can be activated to mediate the generation of Plant Life under Changing Environment

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H2O2 in plant roots (Voothuluru and Sharp, 2013). For instance, Wei et al. (2015) verified that the expression of wheat OxOx-coding genes significantly affected cell osmosis and ROS metabolism (especially H2O2) and enhanced the tolerance of transgenic Arabidopsis response to plant fungus such as white mold. As a single-gene product in a separate and interchangeable form, xanthine dehydrogenase (XDH) produces NADH instead of O
2 and uric acid using hypoxanthine 2 or xanthine as a substrate in the case of NAD1 as a cofactor [xanthine 1 NAD1 1 H2O3uric acid 1 NADH 1 H1; 2xanthine 1 2H2O 1 O232uric acid 1 H2O2 (or hypoxanthine 1 H2O 1 2NAD13uric acid 1 2NADH 1 H1)] (referred by Zarepour et al., 2010; Ma et al., 2016; Hofmann, 2016). Upon specific conditions, this enzyme can also be converted to xanthine oxidase (XAO) (Wang et al., 2016). In animals, XAO is verified as a key oxidative enzyme in the production of ROS (especially for O
2 2 and H2O2) and RNS/•NO, the increase of which could cause oxidative stress and metabolic disorders (Kontos, 1990; Watanabe et al., 2014). In abiotic-stressed Arabidopsis, however, XDH has an important influence on plants’ defense response by regulating the delicate equilibrium between ROS production in epidermal cells and ROS consumption in mesophyll cells (Ma et al., 2016). To date, the structural complexity and specialized tissue distribution of XDH/XAO as well as its high level of regulation indicate that other functions are not yet fully defined and hence require further investigations to elucidate.

14.2.5 Other sources In addition to the sites mentioned earlier, endoplasmic reticulum, cytoplasm, and plasma membrane in plant cells also participate in the production of ROS. Among these, cytochrome P450 (CytP450) is regarded as a ROS resource that mediates detoxification in the cytoplasm and endoplasmic reticulum (ER), which is yet to get attention (Gill and Tuteja, 2010). Its electron transfer can be regulated by NAD(P)H, which combines with 2 CytP450 for the production of O
2 2 in the ER. The CytP450-R , which reduces the flavor protein with the organic substrates RH and CytP450, can form an oxygen-containing complex CytP450-ROO2 in the cytoplasm when reacted with triplet oxygen (3O2; Mittler, 2002; Sagi and Fluhr, 2006; Rezende et al., 2017). NOX as a source of ROS production located in the plasma membrane as RBOHs for respiratory burst oxidase homologs, which can catalyze the production of superoxide (Dubiella et al., 2013; Hyodo et al., 2017). Recently, NOXs have also received increasing attention in the scientific community due to its gene expression and the existence of different homologs under stress conditions. As a part of the ROS production system, these oxidases often induce O
2 2 production by shifting electrons from cytosolic NADPH to O2 or disproportionate the O
2 2 to H2O2 by the effects of SODs (Apel and Hirt, 2004; Jaspers and Kangasja¨rvi, 2010). Earlier, several studies have confirmed that approximately 10 of RBOHs coding genes, and their isoforms have identified from Arabidopsis plants participating in different physiological and signaling processes (Pourrut et al., 2008; Dubiella et al., 2013). For example, RBOH-C is responsible for root-hair growth and mechanical sensing, while RBOH-D/-F function in the signaling transduction of abscisic acid under

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abiotic stresses (Suzuki et al., 2011; Baxter et al., 2014; Yamauchi et al., 2017). Moreover, cytoplasmic Ca21 spiking is considered as a part of the elicitor-induced defense response prior to NOXs activation in plants (Zhao et al., 2005; Wi et al., 2012). In 25 minutes, dynamic cytoplasmic Ca21 spiking induced by elicitors derived from a resting levels of 50100 to 15 μM in tobacco (Nicotiana plumbaginifolia L.) cells (Lecourieux et al., 2002), suggesting that Ca21 may directly trigger the activation of RBOHs. Furthermore, AtRBOH-C participated in the inactivation of Ca21 channels dependent on ROS during root-hair growth (Monshausen and Gilroy, 2009; Kurusu et al., 2015), whereas AtRBOH-D and AtRBOH-F in ABA-induced guardian Ca21-channel activation (Sagi and Fluhr, 2006; Hyodo et al., 2017). These findings indicate the presence of ROS motifs in repeated transduction of calcium signaling. Therefore the complexity of ROS response to various abiotic stresses may be due, at least in part, to the regulatory mechanisms of ROS induced by RBOHs, which play a role in organ type and developmental stages. However, how the ROS waves combine with the pressure-specific signaling of RBOHs is an open question for further investigations.

14.3 Antioxidants involved in stress-induced regulation of reactive oxygen species In the evolutionary process, plants have developed some “complex actions” for managing ROS via the regulation of antioxidant system (Dietz et al., 2016; Liu et al., 2016a,b, 2018). Antioxidants, an important part of the ROS defense mechanism, contributes to relieve the oxidative stressinduced damage and directly related with plant development, which often contains enzymes and nonenzymatic components (Del Rı´o et al., 2002; Choudhury et al., 2013; Liu et al., 2015a,b,c,d; Zhu, 2016; Wu et al., 2017). Among them, antioxidant enzymes play a key role in maintaining cell homeostasis and antioxidant responses in plants. Two types of antioxidant enzymes exist in different cellular compartments: (1) enzymes that participate in various antioxidant activities, such as SOD, catalase (CAT), POD, and phospholipid-hydroperoxide GSH peroxide (PHGPX); (2) specific enzymes that are involved in the ascorbateGSH cycle such as GSH reductase (GR), guaiacol POD (GPX), APX, GSH S-transferases (GSTs), dehydroascorbate reductase, monodehydroascorbate reductase (MDAR), and polyphenol oxidase (PPO; Table 14.2). Correspondingly, nonenzymatic antioxidants are also reported in almost all cellular compartments, which act directly on ROS to detoxify or to reduce the substrate of antioxidant enzymes. These antioxidants mainly include tocopherols (α, β, γ, and δ), ascorbic acid (AsA), reduced GSH, carotenoids, phenolics, flavonoids, and amino acids/AA (such as ARG; histidine/HIS, and proline/PRO) (Das and Roychoudhury, 2014; Hasanuzzaman et al., 2017; Liu et al., 2015a,b,c,d, 2016a,b, 2018). Many studies have now demonstrated that the regulation of antioxidants in plant cells is important for resisting various stresses (Fig. 14.2). Abiotic stress can severely reduce the activity or level of some antioxidants in plant cells, while other antioxidants increase at different levels. Therefore the delicate balance between ROS production and antioxidant regulation is critical for plant growth and development.

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FIGURE 14.2 The antioxidant systems in plants under abiotic stress involved in the detoxification of ROS through a variety of metabolic pathways. 3O2, Triplet oxygen; APX, ascorbate peroxidase; AsA, ascorbic acid; DHA, docosahexaenoic acid; DHAR, dehydroascorbate reductase; GR, glutathione reductase; GSSG, glutathione disulfide; GSH, reduced glutathione; H2O2, hydrogen peroxide; HO2•, hydroperoxy; MDA, malondialdehyde; MDHAR, monodehydroascorbate reductase; NADPH, nicotinamide adenine dinucleotide phosphate; O
2 2 , superoxide radical; OH•, hydroxyl radical; PSI, photosystem I; RO•, alkoxy radical; ROO•, peroxy radical; ROS, reactive oxygen species; SOD, superoxide dismutase. Source: Modified from Choudhury, S., Panda, P., Sahoo, L., Panda, S. K., 2013. Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav. 8, e23681. Available from: https://doi.org/10.4161/psb.23681; Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909930.

14.3.1 Enzymatic antioxidants Metalloenzyme SOD, distributed in almost all aerobic bio-subcellular compartments, is considered to be the most potent intracellular enzyme for the regulation of oxidative stressinduced by ROS (Choudhury et al., 2013). Furthermore, SODs can be divided into three groups based on their metal cofactors: Fe-SOD in chloroplasts, Cu/Zn-SOD in chloroplasts and cytoplasm, and Mn-SOD in mitochondria and peroxisomes (Suzuki et al., 2011; Choudhury et al., 2013). Earlier, Kliebenstein et al. (1990) have identified a Mn-SOD gene (MSD1), three Cu/Zn-SOD (CSD13), and Fe-SOD genes (FSD13) in Arabidopsis plants (A. thaliana L.), respectively, which have also been cloned from various plants in recent years. In particular, the enhancement of SOD activity is a common physiological response against oxidative stress caused by abiotic stress during plant survival and maintenance of normal life activities (Wu et al., 2017). For example, significant increases in activities of SOD have been recorded in various salt-induced plants such as garden tomato ´ (Lycopersicum esculentum Mill.) (Mittova et al., 2003; Gapinska et al., 2008), Chinese cabbage (Brassica campestris L.) (Tseng et al., 2007), peanut cultivar (Arachis hypogaea var. JL-24)

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(Negi et al., 2015), and common sunflower (Helianthus annuus L.) (Arora and Bhatla, 2017). In addition, the increase in TaMnSOD activity of Mn-SOD gene from Tamarix androssowii Litv. was found in salt-stressed transgenic plants (Poplar davidiana 3 Populus bolleana) (Wang et al., 2010a,b). This finding also verifies that SODs have a significant role on improving plant salt tolerance. Moreover, increasing SOD activities were also found following metals treatments in Cd/Cu-stressed white clover (Trifolium repens L.) (Liu et al., 2015b,c,d, 2016a), lead/Pb-poisoned water hyacinths [Eichhornia crassipes (Mart.)] (Malar et al., 2016), and Cd-induced A. thaliana L. (Liu et al., 2018). In various plants, similarly, an enhancement in SOD level was also reported under other stress conditions, such as drought (Negi et al., 2015), water (Voothuluru and Sharp, 2013), heavy metals (Wu et al., 2017), UV-B radiation (Hui et al., 2015), and high and low light (Liu et al., 2015a, 2016b), while decrease or not being affected in SOD levels were recorded in some stress-induced plants (Das and Roychoudhury, 2014). At the molecular level, Yang et al. (2012) investigated the molecular response mechanism of plantain (Musa paradisiaca L.) to cold stress using proteomics techniques at the global scale. The results showed that the molecular mechanism of higher cold tolerance found in plantains can be associated with increased antioxidants (e.g., SOD, CAT, and lypoxygenase/LOX) with adaptability of ROS scavenging, reduction in ROS production and lipid peroxidation. CAT, an antioxidant enzymecontaining tetrameric heme, is essential for the detoxification of ROS under stress conditions. In general, it could directly decompose H2O2 into H2O and O2 as following equation: H2O2-H2O 1 1/2O2. In peroxisomes, CATs could effectively remove H2O2 produced by beta-oxidation involved in photorespiration processes, sputum catabolism, and FAs (Gill and Tuteja, 2010). Currently, several isoenzymes of CATs (e.g., CAT13) and their functions have also been identified from different higher plants. Typically, CAT12 are distributed in peroxisomes and cytosols, while CAT3 is found in mitochondria. Ali and Alqurainy (2006) reported that CATs may interact with some hydroperoxides such as methyl hydroperoxide under specific stress conditions. Previous studies have shown that CAT isoenzymes are regulated in time and space and may respond differently to light (Willekens et al., 1994; Liu et al., 2015a, 2016b), salt (Wang et al., 2010a,b; Negi et al., 2015), and heavy metals (Liu et al., 2015b,c,d, 2016a, 2018; Malar et al., 2016; Wu et al., 2017). Under different abiotic stresses, these discrepancy outcomes of CATs’ levels result from the differences in plant materials, treatment doses, and exposure time, which contribute to plant response to these stresses for the survival of plants (Liu et al., 2015c, 2016a, 2018). Other important antioxidant enzymes are derived from the ascorbateGSH cycle system. For example, APX participates in the removal of H2O2 from waterwater reaction by using AsA as an electron donor (i.e., H2O2 1 AA-2H2O 1 DHA;AA, ascorbic acid; DHA, docosahexaenoic acid). Therefore APX is important for scavenging ROS and maintaining the normal life span of plant cells. At least five isoforms in APX family were reported based on different amino acids and their locations. Sharma and Dubey (2004) have identified three soluble isoforms (i.e., APX, mitAPX and sAPX) from cytosol, mitochondria, and chloroplast matrices, respectively, while two membrane-bound isoforms, that is, mAPX and tAPX are presented in microbodies (peroxisome and glyoxisome) and chloroplast thylakoids. Within the N-/C-terminal protein regions, the subcellular localization of isozymes determined by the existing of organelle-specific targeting peptides and transmembrane domains (Kangasja¨rvi et al., 2008; Caverzan et al., 2012). The isoenzyme-encoding genes in chloroplast APX (chlAPX) were composed of two groups. (1) The first group is a Plant Life under Changing Environment

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gene-encoding two isozymes by the regulation of posttranscriptional splicing, which are authenticated from common spinach (Spinacia oleracea L.), cultivated tobacco (Nicotiana tabacum L.), and ice plants (Mesembryanthemum crystallinum L.) (Ishikawa and Shigeoka, 2008; Pandey et al., 2017 and refs therein). (2) Different isozymes encoded by a single gene are individually regulated in the second group, including genes from tomato, rice (e.g., APX gens OsAPX18), and Arabidopsis plants (A. thaliana; e.g., APX gens AtAPX16, sAPX, tAPX, and lAPX) (Caverzan et al., 2012). Earlier, Ishikawa and Shigeoka (2008) revealed the mechanism of alternative splicing through the investigation of the chlAPX in spinach (S. oleracea L.). Result showed that the alternative splicing can largely control the expression of sAPX and tAPX isoenzymes, which may take place in a tissue-dependent manner. Similar to SOD and CAT, the expression of the APX-encoding gene is also modulated by various abiotic conditions including extreme temperature, photooxidative damage, metal cytotoxicity, and salt and drought stresses (e.g., Sharma and Dubey, 2004; Caverzan et al., 2012; Pandey et al., 2017; Liu et al., 2018). Most of the data collected indicate that the APX subtype in plants has important and direct protective effects against the opposite abiotic environment. Caverzan et al. (2012) strongly believed that different knockdowns or knockouts of APXs have markedly impacts on plant growth and antioxidant metabolism. In the meanwhile, this study also verified that APX may regulate the involvement of plant redox signaling pathways in stressed plants. Similar to the efficacy of APX, GPX could detoxify H2O2 in plant cells to H2O using GSH as a reducing agent (2GSH 1 PUFAOOH-GSSG 1 PUFA 1 2H2O). Several studies (e.g., Leisinger et al., 2001; Choudhury et al., 2013) reported that some differentiated GPX genes could be strongly induced by ROS. For example, the plant GPX gene is highly homologous to mammalian PHGPX and highly sympathetic to lipid hydroperoxides instead of hydrogen peroxide (Foyer and Noctor, 2005a,b; Choudhury et al., 2013, Das and Roychoudhury, 2014 and references therein). In transgenic plants, overexpression of PHGPX also showed stronger abiotic stress tolerance (Foyer and Noctor, 2005a,b; Gill and Tuteja, 2010). GR is one of the flavoprotein oxidoreductases present in higher plants, while MDHAR is a FAD enzyme presenting in the chloroplast and cytoplasm in the form of isozymes. Chalapathi Rao and Reddy (2008) stated that GR has significant influence on maintaining the GSH pool, which mainly due to the reduction of GSH by an NADPH-dependent reaction that catalyzes the GSSG disulfide bonds. In addition, GR is associated with the defense of plant oxidative stress, while GSH activates sulfhydryl (2SH) substrates and GSTs in the cellular system to participate in the ascorbateGSH cycle. Among them, GSTs can catalyze the binding of electrophilic substrates to tripeptide GSH. For the stress tolerance of both, different findings were reported in stressed plants such as Cd-poisoned common pepper (Capsicum annuum L.) (Leon et al., 2002), salt-stressed chickpea plants (Cicer arietinum L. cv. Gokce) (Eyidogan and Oz, 2005), and light-induced Taiwan alder [Alnus formosana (Burkill) Makino] (Liu et al., 2015a, 2016b). As an electron acceptor monodehydroisosorbide (MDHA), however, MDHAR is often used as an electron donor because of its high specificity, preferably NADH instead of NADPH. It has been confirmed that disproportionation of photodegraded ferredoxin (or named Fdred) in thylakoids is a very major mechanism for photosynthetic plants. Compared to NADP1, Fdred could reduce MDHA more effectively. However, MDHAR couldn’t involve in the degradation of MDHA in the thylakoid-clearing systems, which therefore only works only in the presence

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of NADPH (Fdred didn’t; Wise and Naylor, 1987; Wang et al., 2010a,b; Johnston et al., 2015). Schutzendu¨bel et al. (2001) found that an obvious rise in MDHAR activity was found in Cd-exposed pine (Pinus sylvestris L.), but the opposite finding in Cd-induced poplar hybrids (Populus 3 Canescens). Previous publications have also reported that the increased activity of MDAR contributes to normal or transgenic plants in response to drought damage, extreme temperature, salt induction and 2,4,6-trinitrotoluene stress (e.g., Stevens et al., 2008; Yin et al., 2010; Sandalio et al., 2013; Liu et al., 2016a).

14.3.2 Nonenzymatic antioxidants Ascorbic acid (AsA) is a multifunctional and widely regulated antioxidant involved in balancing damage caused by abiotic stress in the ascorbateGSH cycle. Most of the AsA is produced by the catalysis of L-galactose-γ-lactone dehydrogenase (GLDase) in the plant mitochondria (defined as the “Smirnoff-Wheeler” pathway), while the remaining is produced by D-galacturonic acid (Linster et al., 2007; Badejo et al., 2009). In high plants, AsA is generally oxidized in two consecutive steps, starting with oxidation to MDHA, otherwise disproportionation to ascorbic acid and DHA. Moreover, AsA could react with active oxygen (e.g., hydrogen peroxide and superoxide ions) to regenerate α-tocopherol from the propoxy group (CHEBI: 46881), thereby oxidative damage to the normal metabolism of the cell membrane (Za´dor and Miller, 2013; Das and Roychoudhury, 2014). Under abiotic stress, AsA also participated in the regulation and response of abiotic stress poisoning in plant cells. In our previous studies, for instance, the reduction or increase of AsA levels was observed in Cu/Cd-induced plants (Liu et al., 2015a,b,c,d, 2016a, 2018). Malik and Ashraf (2012) reported that the addition of AsA exogenously improved the growth and development in drought-stressed wheat (Triticum aestivum L.). Compared to control, plants supplemented with AsA showed higher net photosynthetic rate (Anet), transpiration rates (Tr), and stomatal conductance (Gs), resulting in an increase in photosynthesis. Complementarily, exogenous AsA reduces salt-induced oxidative damage in wheat plants, mainly by increasing photosynthetic capacity and maintaining ion homeostasis (Athar et al., 2008). In addition, drought stress markedly enhanced the levels of AsA and the activities of various antioxidants in spruce (or Chinese spruce, Picea asperata Mast.) under high-light stress. Yang et al. (2008) observed a significant cross-linking between drought and low-light conditions, corresponding to a delicate balance between antioxidants and ROS (i.e., H2O2 and O
2 2 ). Moreover, Rybarczyk-Plonska et al. (2014) pointed out that various postharvest factors (e.g., high/low light, extreme temperature, and UV-B radiation) significantly affected the concentration of AsA in the flower buds of broccoli (Brassica oleracea L. var. italica). Recent investigations also indicated that UV-B radiation clearly affected the accumulation of AsA, phenolics, and flavonoids in mung beans [Vigna radiata (L.) R. Wilczek], strongly linking with the alterations in the activities of enzymatic antioxidants such as POD, PPO, GLDH, phenylalanine ammonia-lyase, and chalcone isomerase (Das and Roychoudhury, 2014; Rybarczyk-Plonska et al., 2014; Wang et al., 2017). In contrast, a decrease in the AsA concentration in Cd-stressed white clover (T. repens L.) shoot (Liu et al., 2015b) and Cu-induced Madagascar periwinkle (Catharanthus roseus L.) tissues (both leaves and roots; Liu et al., 2016a) was recorded in our previous

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investigations. An interesting finding showed a significant increase in antioxidants and glyoxalase-pathway enzymes (glyoxalase I and II), as well as a higher ratio of GSH and GSSG, which prevented the accumulation of the potent cytotoxic compound methylglyoxal. It ultimately causes the increase in salt tolerance of the transgenic potato (Solanum tuberosum L.), accompanied by a higher AsA level from the overexpression of GalUR (Upadhyaya et al., 2011). In the ascorbateGSH cycle, tripeptide GSH (γ-glutamyl-cysteinyl-glycine; GSH), one of the other key metabolites distributed in plant chloroplasts, cytoplasm, and mitochondria (Zechmann and Mu¨ller, 2010; Das and Roychoudhury, 2014), is regarded as a key intracellular defense against the oxidative damage induced by ROS (Hasanuzzaman et al., 2017). In general, two ATP-dependent steps contribute to the synthesis of GSH: (1) the γ-glutamylcysteine formed from two amino acid [cysteine (CYS) and glutamic acid] catalyzed by the glutamateCYS ligase (rate-limiting step); and (2) addition of glycine acid to γ-glutamylcysteine for the production of GSH via GSH syntheses (Mahmood et al., 2010; Foyer and Noctor, 2013; Rybarczyk-Plonska et al., 2014; Xia et al., 2015). In the ascorbateGSH cycle, besides, GSH involves in antioxidant defense systems by recycling the potential water-soluble antioxidants. As a key molecule against oxidative stress, GSH has an irreplaceable role in the removal of abiotic stress-activated ROS. Karaly-Salama and Al-Mutawa (2009) reported that GSH acts as a ROS scavenger to regulate plasma membrane changes in epidermal cells in salt-induced onion plants (Allium cepa L.). Wu et al. (2014) also found that the addition of 6-benzyladenine exogenously increased the levels of enzymatic (SOD and POD) and nonenzymatic antioxidant (AsA, GSH, and PRO) but decreased the concentrations of O
2 2 and malondialdehyde (marker for oxidative stress) in salt-stressed eggplant plants (Solanum melongena Mill.). In addition, previous studies have reported that increased levels of endogenous GSH confer drought stress tolerance, thereby attenuating ROS-induced damage. For instance, Alam et al. (2013) stated that salicylic acid (SA) applied exogenously had a beneficial influence for relieving the drought-induced oxidative stress, resulting from the enhancement of the stress tolerance by increasing the proportion of reduced oxidized GSH and activities of ascorbateGSH cycle antioxidants including endogenous GSH. Similarly, higher levels of GSH confer high-temperature tolerance by efficient elimination of ROS in various plants such as common wheat (T. aestivum L.), common beech (Fagus sylvatica L.), and maize (Zea mays subsp.) (Hasanuzzaman et al., 2017 and references therein). Besides, Luo et al. (2011) revealed, in the ascorbateGSH cycle, higher GSH and enzymes levels also increased the tolerance of the strawberry (Fragaria ananassa Duch.) species exposed to low-temperature stress. Interestingly, in our previous works, Cu stress increased the GSH level in the shoots but decreased in the roots of Madagascar periwinkle (C. roseus L.) (Liu et al., 2016a). However, the exogenously added NO donor SNP (sodium nitroprusside) effectively offsets the consumption of GSH and AsA by Cu, suggesting that NO may participate in the detoxification of ROS through ascorbateGSH cycle (Liu et al., 2015b,c,d). The level of oxidative stress is mainly determined by the balance between ROS production and clearance, which is also essential for maintaining a balanced redox state (Choudhury et al., 2013; Vaahtera et al., 2014; Rybarczyk-Plonska et al., 2014; Liu et al., 2015b,c,d). The function of GSH as an antioxidant imparting abiotic stress tolerance has been well established and proved by many previous investigations. Therefore future research will require the identification of genes





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responsible for GSH biosynthesis and cellular mechanisms that regulate enzymes involved in GSH metabolism or degradation.

14.4 Signaling roles of reactive oxygen species in plants under abiotic stress 14.4.1 Reactive oxygen species signal perception Due to the widespread distribution of ROS molecules in aerobic plants, cells have the capability to specifically decode the ROS signaling for different ROS-containing species, time coordination and subcellular localization (Jaspers and Kangasja¨rvi, 2010; Murphy et al., 2011; Herna´ndez-On˜ate et al., 2012; Wang et al., 2012; Dietz et al., 2016; MignoletSpruyt et al., 2016). To date, many publications have proposed different mechanisms to describe the specificity of ROS perception. In general, these mechanisms predominantly include (1) the perception and oxidation of the resulting oxylipins (Wise and Naylor, 1987; ´ Pastore et al., 2002; Gapinska et al., 2008; Tripathy and Oelmu¨ller, 2012; Wrzaczek et al., 2013), (2) the monitoring of cellular redox status (Chalapathi Rao and Reddy, 2008; Chang et al., 2010; Brosche´ and Kangasja¨rvi, 2012; Corpas et al., 2017a,b), and (3) the direct oxidation modification of proteins located on the residues of CYS, selenocysteine (SEC or SeCys), or methionine (Morgan et al., 2012; Foyer and Noctor, 2005a,b, 2009, 2013; Vaahtera et al., 2014). Previous publications also described that other amino acids, such as HIS, tryptophan, tyrosine (TYR), valine, and PRO, could be modified by oxidized form (Liu et al., 2012; Houe´e-Le´vin et al., 2015); however, the relevance of these modifications requires further investigations. Some specific proteins with oxidative-damage properties were rapidly targeted by proteasome degradation through autophagy pathways, which is an intracellular degradation process that delivers cytoplasmic components to vacuoles during stress process (Han et al., 2011; Herna´ndez-On˜ate et al., 2012). However, oxidized and denatured proteins are still able to exert signal functions in plant cells prior to degradation; therefore the perception of ROS cannot be excluded. As one of the best examples, Wu et al. (2012) verified that the redox-regulated signaling proteins in plants are the interaction of the TGACGTCA cis-element-binding-protein transcription factors with the coactivator NPR1. In general, NPR1exists as an oxidized multimer in both nucleus and cytoplasm under normal growth conditions (Rochon et al., 2006). However, a portion of the nuclear NPR1 population served as a potential coactivator, which is recruited to the PR-1 promoter under noninducing conditions (Wu et al., 2012). Tada et al. (2008) found that changes in the redox state of thioredoxin resulted in a decrease in NPR1, and then the monomers released by them were transferred to the nucleus. Lindermayr et al. (2010) concluded that NPR1 and its interactants such as TGA1 are S-nitrosylated at the CYS residue. More interestingly, both proteins were modified by GSNO to increase the DNA-binding activity of TGA1, which at least partially indicated that NO was committed to the regulation of the Arabidopsis NPR1TGA1 system. This also provides important evidence for the redoxcontrol mechanism of plant defense responses (Liu et al., 2018). Furthermore, Yun et al. (2011) reported that NO also can control a negative feedback loop that limits allergic reactions when the concentration of SNO was high. This process is often mediated by Snitrosylation of the NADPH oxidase, and Arabidopsis RBOH isoform D (AtRBOH-D) at





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Cys 890 (one of the two CYSs at the C-terminal portion of AtRBOH-D; Lindermayr et al., 2010; Kimura et al., 2012; Kurusu et al., 2015), thus quenching its ability of ROS intermediates synthesis. Accordingly, mutations of the Cys 890 compromised SNO-mediated control of the AtRBOH-D activity and disturbing the extent of cell-death progression. The CC-type glutaredoxin (GRX) is also an important TF that directly participates in redox regulation. Murmu et al. (2010) described that two Arabidopsis GRXs genes ROXY1 and ROXY2 redox-regulated the basic leucine zipper TGA-group TFs TGA9 and TGA10, as well as modified the CYS residues for promoting anther development. In addition, the transcription factor RAP2.4a (associated with AP2 4a) is regulated by redox, which establishes a redox-regulated transformation mechanism for the nuclear genes of chloroplast antioxidants. Among them, RAP 2.4 is regarded as a redox sensor and converter (Shaikhali et al., 2008). Under heat stress, A. thaliana heat shock factor HsfA1a has been identified as a direct perception of heat shock, hydrogen peroxide, and pH changes through the participation of redox states (Liu et al., 2013). Nevertheless, some regulated proteins by oxidative modification of AA in plants were reported. For example, ATPases (i.e., V-type ATPases) were transported by two-component system RegB/RegA and vacuolar protons. Wu et al. (2013) reported that RegB kinase activity is inhibited by oxidation of CYS sulfate, while RegA phosphorylation regulates gene expression by affecting the interaction of RegA with promoter and RNA polymerase. As a redox switch, Cys 265 controls the kinase activity of RegB to form a variety of thiol modifications in response to redox signals. Besides, V-type ATPase is a nanoscale molecular machine that performs rotational catalysis to drive protons across the membrane (Liu et al., 2015b,d). Seidel et al. (2012) found that the oxidation inhibition of ATP hydrolysis and proton transport is mainly prevented by C256S substitution in VHA-A of Arabidopsis plants. However, the oxidative inhibition of the plant V-type ATPase does not involve the formation of intramolecular disulfide bonds within VHA-A, as is proposed for both yeast and mammals.

14.4.2 Transduction and Interaction of reactive oxygen species signaling Many ROS-sensing factors in plant cells have been identified; however, transductions of extracellular ROS under stress conditions have not been well described. Many previous studies have revealed key components involved in plant ROS signaling (especially the model plant Arabidopsis; Dickinson et al., 2011; Baxter et al., 2014). There are three mechanisms for sensing ROS signaling in plants: invalidated receptor-protein action, redox-sensitive transcription factor, and direct inhibition of ROS in phosphatases (Apel and Hirt, 2004; Jaspers and Kangasja¨rvi, 2010; Sinha et al., 2011; Foyer and Noctor, 2013; Mittler, 2017). Among them, the mitogen-activated protein kinases (MAPKs) cascades involve in the transduction of extracellular signaling from cell membrane to nucleus via the phosphorylation event cascade, which are negatively regulated by the MAPK phosphatases (Jaspers and Kangasja¨rvi, 2010; Choudhury et al., 2013; Foyer and Noctor, 2013). In a general model the MAPK cascade consists of at least three kinases, namely, MAPK (MAP kinase or MPKs), MAP2Ks (MAP kinase kinase; or MAPKK, MEK, and MKK), and MAP3Ks (MAP kinase kinase kinase; or MAPKKKs and MEKKs; Rodriguez et al., 2010). Among these, MAP3Ks are SER (Serine) or THR (Threonine) kinases, which phosphorylate

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MAP2Ks at a conserved S/T-X3-5-S/T motif. However, MAP2Ks phosphorylate THR and TYR kinases at a conserved T-X-Y motif (Chang and Karin, 2001; Rodriguez et al., 2010). In addition, MAP4Ks (MAP kinase kinase kinase kinases) act as an adapter that links with the upstream signaling step of the core MAPK cascade. In higher plants the MAPKs cascade are induced by various abiotic stress such as extreme temperatures, ozone stress, UV radiation, salt stress, mechanical wounding, and metals toxicity (Chang and Karin, 2001; Jaspers and Kangasja¨rvi, 2010; Son et al., 2011; Xu and Zhang, 2015), which, therefore, play a role in a variety of signal-transduction pathways. For example, stimulating plasma membrane activates MAP3K or MAP4K under abiotic environmental stress (Sinha et al., 2011). In addition, in the model Arabidopsis plants, a large number of MAPKs cascades provide a range of crosstalking between/among different stress signals. Further, many different MAPKs cascades are activated by the accumulated ROS in plant cells, which include the ROS-responsive MAP3Ks (or MEKKs; e.g., MEKK1), MAP2Ks(e.g., MKK2), and MPKs (e.g., MPK4, MPK9, and MPK12) (Teige et al., 2004; Jammes et al., 2009; Mittler et al., 2011 and references therein). The MEKK1 pathway, an activator of two highly homologous MAPKKs (i.e., MKK1 and MKK2), exhibits higher activities at the upstreams of MAPKs, MPK4 and MPK6 under abiotic/oxidative stress (Nakagami et al., 2006; Xu et al., 2008; Xu and Zhang, 2015). Xing et al. (2008) also found that CAT1 expression and ROS production are affected by AtMKK1. Moreover, AtMKK1 is involved in the transmission of AtMPK6coupled signals in Arabidopsis plants. As a key module, AtMKK1AtMPK6 often result in ROS production and stress responses in the ABA-dependent signaling cascade. Similarly, previous studies have also shown that MPK4 mutants accumulate large amounts of H2O2, indicating that CAT2 activity is induced or stabilized by MPK4 (Chang and Karin, 2001). The level of MEKK1 protein is changed with increase of H2O2, indicating that MEKK1MPK4 participated in ROS regulation as part of the regulatory feedback loop. In addition, MKK2 acts as a key signal transducer to mediate stress signals via the MAPKKKMAPKKMAPK module, which consists of MEKK1MKK2MPK4/MPK6 under salt/cold stress (Teige et al., 2004). Previous studies also reported that two ROS-responsive MAP kinases MPK3 and MPK6 are activated by the ROS molecule H2O2, which are dependent on the activity of MKK9 under abiotic and oxidative stress. Pitzschke and Hirt (2009) confirmed that, unlike CAT1, CAT2 expression participates in SA accumulation for ultimate plant defense through the joint regulation of MEKK1 and MPK4. Moreover, Xu et al. (2008) found that the biosynthesis of ethylene (ET) and camalexin (3-thiazole-20 -yl-indole) in Arabidopsis plants is closely related to the regulation of MKK9MPK3/MPK6 cascade, which may be the key axis of stress response. In ozone-stressed Arabidopsis, initial AtMPK3 and AtMPK6 activation in response to ozone is not independent of ET signaling, but ET may have a secondary influence on AtMPK3 and AtMPK6 functions, whereas functional SA signaling is required for full-level AtMPK3 activated by ozone (Ahlfors et al., 2004). Furthermore, Lumbreras et al. (2010) reported that MKP2 participate actively in the regulation of stress oxidation. Therefore the MAPKs pathway has an important implications for the transformation and/or transduction of ROS signaling into protein phosphorylation (or corresponding signaling) in plants’ abiotic stresses. Unlike MAPKs, hormonal signaling such as ET, SA, and ABA are driven assembly by the transduction of different signaling pathways in plant cells (Ma et al., 2012). It is worth

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mentioning that ABA contribute to a large number of bio-signal functions and has significant binding effects with ROS signaling (Sagi and Fluhr, 2006; Rezende et al., 2017; Yamauchi et al., 2017). Response to heat stress, for example, plant systemic acquired acclimation (SAA) is closely related to the activation of ROS signaling and the instantaneous accumulation of hormone ABA in tissues, although it is inhibited when lacking RBOH-D in mutants (Suzuki et al., 2013). These findings also revealed a significant spatiotemporal interactions between ABA-mediated SAA and RBOH-D-dependent ROS in response to heat stress. In the early 1990s Chen et al. (1993) reported for the first time a feed-forward loop between ROS production and SA signaling in the defense responses. Later studies confirmed that ROS signaling contributes to the upstream and downstream of SA signaling in response to abiotic stresses such as drought stress (Wan et al., 2012), high-light damage (Mateo et al., 2006), high-salt induction (Lee and Park, 2010; Miura and Tada, 2014), extreme temperature (Khan et al., 2013; Miura and Tada, 2014), and heavy metal cytotoxicity (Liu et al., 2015c,d; Tama´s et al., 2015). For instance, SA indirectly attenuate Cd-stressed damage by the inhibition of IAA-mediated ROS production in soybean roots (Tama´s et al., 2015), whereas SA directly reduce heat stress by the regulation of PRO/ET synthesis in wheat (Khan et al., 2013). In our previous study, we also observed that NO contributes to counteract the oxidative stress caused Cd toxicity through stress-related hormones (Liu et al., 2015c,d). An interesting finding is, in Cd-stressed white clove plants (T. repens L.), SA levels in the shoots were not changed by the additions of various NO modulators, such as NO donors SNP, NO scavenger cPTIO (carboxy-PTIO potassium salt) and NOS inhibitor L-NAME (L-NG-nitroarginine methyl ester). On the contrary, Arasimowicz-Jelonek et al. (2012) found that cPITO could significantly inhibit the synthesis of SA in Cd-stressed lupin (Lupinus micranthus Guss.) leaves. One possible explanation for this difference is that the synthesis of SA may be impaired in genetic defects under abiotic stress conditions, although the relationship between NO and SA is closely related to plant defense (Feechan et al., 2005). Interestingly, Seyfferth and Tsuda (2014) recently proposed that Ca21 signaling is able to regulate the production of SA in plants, which is based on this fact that activities of the factors, such as CaM-binding transcription activators (CAMTA3) (Du et al., 2009), CaM-binding protein 60G (CBP60) (Truman et al., 2013), and WRKY8/28/48 (Gao et al., 2013), are regulated by CaM and CDPKs and CaMKs. Therefore the possibility that Ca21 signaling mediates activation of SA that induced by ROS production is an interesting aspect of exploration. For ET, Jakubowicz et al. (2010) verified that ET biosynthesis was found to be positively regulated by the RBOH protein but negatively regulated by CTR1 (constitutive triple response 1). In detail, phosphatidic acid derived from PLD can directly affect the ET-signal-transduction pathways by inhibiting the activity of CTR1 and activation of RBOH-D/-F (Jakubowicz et al., 2010). In our previous work, SNP depleted the increase in the level of ET induced by Cd stress in white clover plants, suggesting that the activity of Met adenosyl transferase-1 can be changed by S-nitrosation regulation (Liu et al., 2015c). Besides, NO could inhibit the formation of ET in plant cells by reducing the synthase or oxidase of activities of 1-aminocyclopropane-1-carboxylic acid (Lindermayr et al., 2006). It has also been shown that there is a significant association between iron-related genes upregulated by ET and NO. However, iron deficiency is capable of upregulating genes (AtETR1, AtCTR1, and AtEIN2) for ET synthesis and signaling transductions in Arabidopsis roots (Garcı´a et al., 2010; Liu et al., 2018). Therefore ROS signaling is often













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highly integrated with various hormone signaling networks for allowing plants to regulate developmental processes and to improve the adaptive response to environmental effects.

14.5 Conclusion and future prospects Despite the remarkable development in our understanding of the biological properties of ROS, the exact nature of the ROS-signaling language is still not clearly described. This chapter attempts to explore the regulation role and the signaling pathways of ROS and their interrelationships in response to abiotic stresses. The early description of ROS is considered by most scientists to be a toxic metabolic by-product of aerobic organisms. However, it has now been found to play an active role in complex signaling networks as an important signaling molecule. Recently, a large body of academic literature confirms the contribution of ROS to plant or animal developmental differentiation, physiological metabolism, and stress response. A notable conclusion is that the beneficial effects of ROS in living organisms are significantly higher than those of ROS on biological systems, thereby refocusing on this pressing issue: are ROS good or bad? Definitely, the dependence of aerobic organisms on ROS can be considered to be consistent with a “bell-curve” response, the optimal state of which depends on the developmental stage, the nature of the cells, and the coupling of the environment in the entire plant systems. Therefore too low or too high ROS levels will adversely affect plant growth and development. In other words, keeping plant ROS in the right range can promote plant health, just as adhering to the balance principles of inward and outward. From the point of view of signal perception and propagation, and considering the hypothesis that ROS is employed as an early signal for detecting cellular oxygen levels, it should not be surprising that cell proliferation requires ROS in aerobic organisms. In fact, ROS is a critical component of plant abiotic stress response, which is determined by ROS levels or cellular redox states. At high concentrations cell death begins, whereas ROS initiates defense genes and adaptive responses at low concentrations. Therefore ROS is good for aerobic organisms, but too much or too little will turn out to be bad. There is no doubt that our understanding in the field of ROS has been improved significantly over the past few decades, but we still have a long way to go. Accordingly, in this exciting era of ROS signal development, it also has provided us with a new and more challenging stage to address the open questions into their right place by revealing the new biological roles of ROS. For example, several key questions arise from our perspective, which are as follows: 1. It provides a flexible potential opportunity for ROS with a dual role due to the multiple sources of ROS derivatives and the complex mechanisms of antioxidant functions. However, how do these regulatory systems work at the cellular level to achieve temporal and spatial coordination with ROS signaling? 2. Although other elements of intercellular ROS sensing have been largely established, how do extracellular ROS signals pass through different cells or subcellular sites as well as the exact pathways of perception and transduction among them? 3. Considering the specificity and complexity of the ROS gene network and its interaction with plant signaling networks, how does the ROS-regulated gene network connect with

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other signaling networks, especially the transduction and integration of different signals under stress conditions? 4. How to develop better methods to detect/quantify different types of ROS species and stress markers of aerobic biological systems under abiotic stresses? Currently, new approaches provide more and more technical support for addressing this question, such as genetic methods; however, refocusing on traditional biochemical theories and methodologies of overcoming genetic redundancy are also essential. While, answering these questions, it will be crucial to elucidate the mechanism of ROS signaling in aerobic organisms especially in plants. As described earlier, ROS is associated with many stress responses in various common abiotic stress; therefore the understanding of the perception and transmission of ROS signals will have a significant influence on modern biotechnology and agricultural production. Although significant advance has been made in exploring ROS signal role in plants, the crucial metabolisms of ROS signaling in stress regulationare yet needed to be clear. Therefore future work will undoubtedly reveal the novel signaling role of ROS and its interaction with other important signals, which will be an extremely important and promising work for ROS research.

References Ahammed, G.J., Li, X., Zhang, G., Zhang, H., Shi, J., Pan, C., et al., 2017. Tomato photorespiratory glycolateoxidase-derived H2O2 production contributes to basal defence against Pseudomonas syringae. Plant Cell Environ. Available from: https://doi.org/10.1111/pce.12932. Ahlfors, R., Macioszek, V., Rudd, J., Brosche´, M., Schlichting, R., Scheel, D., et al., 2004. Stress hormone independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J. 40, 512522. Alam, M.M., Hasanuzzaman, M., Nahar, K., Fujita, M., 2013. Exogenous salicylic acid ameliorates short-term drought stress in mustard (Brassica juncea L.) seedlings by up-regulating the antioxidant defense and glyoxalase system. Aust. J. Crop. Sci. 7, 10531063. Ali, A.A., Alqurainy, F., 2006. Activities of antioxidants in plants under environmental stress. In: Motohashi, N. (Ed.), The Lutein-Prevention and Treatment for Diseases. Transworld Research Network, India. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373399. Arasimowicz-Jelonek, M., Floryszak-Wieczorek, J., Deckert, J., Rucinska-Sobkowiak, R., Gzyl, J., Pawlak-Sprada, S., et al., 2012. Nitric oxide implication in cadmium-induced programmed cell death in roots and signaling response of yellow lupine plants. Plant Physiol. Biochem. 58, 124134. Arora, D., Bhatla, S.C., 2017. Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD. Free Radical Biol. Med. 106, 315328. Athar, H.U.R., Khan, A., Ashraf, M., 2008. Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Environ. Exp. Bot. 63, 224231. Atkin, O.K., Macherel, D., 2009. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot. 103, 581597. Badejo, A.A., Fujikawa, Y., Esaka, M., 2009. Gene expression of ascorbic acid biosynthesis related enzymes of the Smirnoff-Wheeler pathway in acerola (Malpighia glabra). J. Plant Physiol. 166, 652660. Baxter, A., Mittler, R., Suzuki, N., 2014. ROS as key players in plant stress signalling. J. Exp. Bot. 65, 12291240. Bhattacharjee, S., 2012. The language of reactive oxygen species signaling in plants. J. Bot. 2012, e985298. Available from: https://doi.org/10.1155/2012/985298. Boguszewska, D., Grudkowska, M., Zagdan˜ska, B., 2010. Drought-responsive antioxidant enzymes in potato (Solanum tuberosum L.). Potato Res. 53, 373382.

Plant Life under Changing Environment

References

345

Brosche´, M., Kangasja¨rvi, J., 2012. Low antioxidant concentrations impact on multiple signalling pathways in Arabidopsis thaliana partly through NPR1. J. Exp. Bot. 63, 18491861. Buchert, F., Forreiter, C., 2010. Singlet oxygen inhibits ATPase and proton translocation activity of the thylakoid ATP synthase CF1CFo. FEBS Lett. 584, 147152. Caverzan, A., Passaia, G., Rosa, S.B., Ribeiro, C.W., Lazzarotto, F., Margis-Pinheiro, M., 2012. Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genet. Mol. Biol. 35, 10111019. Chalapathi Rao, A.S.V., Reddy, A.R., 2008. Glutathione reductase: a putative redox regulatory system in plant cells. In: Khan, N.A., Singh, S., Umar, S. (Eds.), Sulfur Assimilation and Abiotic Stresses in Plants. Springer, The Netherlands. Chang, L., Karin, M., 2001. Mammalian MAP kinase signaling cascades. Nature 410, 3740. Chang, Y.C., Huang, C.N., Lin, C.H., Chang, H.C., Wu, C.C., 2010. Mapping protein cysteine sulfonic acid modifications with specific enrichment and mass spectrometry: an integrated approach to explore the cysteine oxidation. Proteomics 10, 29612971. Chen, S., Dickman, M.B., 2004. Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. J. Exp. Bot. 55, 26172623. Chen, Z., Silva, H., Klessig, D.F., 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262, 18831886. Choudhury, S., Panda, P., Sahoo, L., Panda, S.K., 2013. Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav. 8, e23681. Available from: https://doi.org/10.4161/psb.23681. Corpas, F.J., Barroso, J.B., 2017. Lead-induced stress, which triggers the production of nitric oxide (NO) and superoxide anion (O
2 2 ) in Arabidopsis peroxisomes, affects catalase activity. Nitric Oxide 68, 103110. Corpas, F.J., Barroso, J.B., Palma, J.M., Rodriguez-Ruiz, M., 2017a. Plant peroxisomes: anitro-oxidative cocktail. Redox Biol. 11, 535542. Corpas, F.J., Pedrajas, J.R., Palma, J.M., Valderrama, R., Rodrı´guez-Ruiz, M., Chaki, M., et al., 2017b. Immunological evidence for the presence of peroxiredoxin in pea leaf peroxisomes and response to oxidative stress conditions. Acta Physiol. Plant. 39, e57. Available from: https://doi.org/10.1007/s11738-017-2356-2. Cramer, G.R., Urano, K., Delrot, S., Pezzotti, M., Shinozaki, K., 2011. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 11, e163. Available from: https://doi.org/10.1186/1471-2229-11-163. Das, K., Roychoudhury, A., 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2, e53. Available from: https://doi.org/0.3389/ fenvs.2014.00053. Del Rı´o, L.A., Corpas, F.J., Sandalio, L.M., Palma, J.M., Go´mez, M., Barroso, J.B., 2002. Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J. Exp. Bot. 53, 12551272. Dickinson, B.C., Chang, C.J., 2011. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat. Chem. Biol. 7, 504511. Dietz, K.J., Mittler, R., Noctor, G., 2016. Recent progress in understanding the role of reactive oxygen species in plant cell signaling. Plant Physiol. 171, 15351539. Doyle, S.M., Diamond, M., McCabe, P.F., 2010. Chloroplast and reactive oxygen species involvement in apoptoticlike programmed cell death in Arabidopsis suspension cultures. J. Exp. Bot. 61, 473482. Du, L., Ali, G.S., Simons, K.A., Hou, J., Yang, T., Reddy, A.S., et al., 2009. Ca(2 1 )/calmodulin regulates salicylicacid-mediated plant immunity. Nature 457, 11541158. Dubiella, U., Seybold, H., Durian, G., Komander, E., Lassig, R., Witte, C.P., et al., 2013. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. U.S.A. 110, 87448749. Duong, N.T., Vinh, P.D., Thuong, P.T., Hoai, N.T., Thanh, L.N., Bach, T.T., et al., 2017. Xanthine oxidase inhibitors from Archidendron clypearia (Jack.) I.C. Nielsen: results from systematic screening of Vietnamese medicinal plants. Asian Pac. J. Trop. Med. 10, 549556. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Che´trit, P., Foyer, C.H., et al., 2003. Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15, 12121226. Elstner, E.F., 1991. Mechanism of oxygen activation in different compartments. In: Pell, E.J., Steffen, K.L. (Eds.), Active Oxygen/Oxidative Stress and Plant Metabolism. American Society of Plant Physiologists, Roseville, CA. Eyidogan, F., Oz, M.T., 2005. Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiol. Plant. 29, 485493.

Plant Life under Changing Environment

346

14. Regulations of reactive oxygen species in plants abiotic stress: an integrated overview

Feechan, A., Kwon, E., Yun, B.W., Wang, Y., Pallas, J.A., Loake, G.J., 2005. A central role for S-nitrosothiols in plant disease resistance. Proc. Natl. Acad. Sci. U.S.A. 102, 80548059. Foyer, C.H., Noctor, G., 2005a. Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28, 10561071. Foyer, C.H., Noctor, G., 2005b. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 18661875. Foyer, C.H., Noctor, G., 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11, 861905. Foyer, C.H., Noctor, G., 2013. Redox signaling in plants. Antioxid. Redox Signal. 18, 20872090. Gao, X., Chen, X., Lin, W., Chen, S., Lu, D., Niu, Y., et al., 2013. Bifurcation of Arabidopsis NLR immune signaling via Ca(2)(1)-dependent protein kinases. PLoS Pathog. 9, e1003127. Available from: https://doi.org/10.1371/ journal.ppat.1003127. ´ Gapinska, M., Skɫodowska, M., Gabara, B., 2008. Effect of short- and long-term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots. Acta Physiol. Plant. 30, 1118. Garcı´a, M.J., Lucena, C., Romera, F.J., Alca´ntara, E., Pe´rez-vicente, R., 2010. Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. J. Exp. Bot. 61, 38853899. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909930. Gilroy, S., Bialasek, M., Suzuki, N., Gorecka, M., Devireddy, A., Karpinski, S., et al., 2016. ROS, calcium and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 171, 16061615. Gratao, P.L., Polle, A., Lea, P.J., Azevedo, R.A., 2005. Making the life of heavy metal stressed plants a little easier. Funct. Plant Biol. 32, 481494. Gray, J., Janick-Buckner, D., Buckner, B., Close, P.S., Johal, G.S., 2002. Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol. 130, 18941907. Hackenberg, C., Kern, R., Hu¨ge, J., Stal, L.J., Tsuji, Y., Kopka, J., et al., 2011. Cyanobacterial lactate oxidases serve as essential partners in N2 fixation and evolved into photorespiratory glycolate oxidases in plants. Plant Cell 23, 29782990. Halliwell, B., Gutteridge, J.M.C. (Eds.), 1989. Free Radicals in Biology and Medicine. Clarendon Press, Oxford, England. Halliwell, B., Gutteridge, J.M.C. (Eds.), 2007. Free Radicals in Biology and Medicine. fifth ed. Oxford University Press, Oxford, England. Han, S., Yu, B., Wang, Y., Liu, Y., 2011. Role of plant autophagy in stress response. Protein Cell 2, 784791. Hasanuzzaman, M., Nahar, K., Anee, T.I., Fujita, M., 2017. Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol. Mol. Biol. Plants 23, 249268. Herna´ndez-On˜ate, M.A., Esquivel-Naranjo, E.U., Mendoza-Mendoza, A., Stewart, A., Herrera-Estrella, A.H., 2012. An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc. Natl. Acad. Sci. U.S.A. 109, 1491814923. Ho, L.H., Giraud, E., Uggalla, V., Lister, R., Clifton, R., Glen, A., et al., 2008. Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis. Plant Physiol. 147, 18581873. Hofmann, N.R., 2016. Opposing functions for plant xanthine dehydrogenase in response to powdery mildew infection: production and scavenging of reactive oxygen species. Plant Cell 28, e1001. Available from: https:// doi.org/10.1105/tpc.16.00381. Houe´e-Le´vin, C., Bobrowski, K., Horakova, L., Karademir, B., Scho¨neich, C., Davies, M.J., et al., 2015. Exploring oxidative modifications of tyrosine: an update on mechanisms of formation, advances in analysis and biological consequences. Free Radical Res. 49, 347373. Hu, W.H., Song, X.S., Shi, K., Xia, X.J., Zhou, Y.H., Yu, J.Q., 2008. Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46, 581588. Hui, R., Li, X., Zhao, R., Liu, L., Gao, Y., Wei, Y., 2015. UV-B radiation suppresses chlorophyll fluorescence, photosynthetic pigment and antioxidant systems of two key species in soil crusts from the Tengger Desert, China. J. Arid Environ. 113, 615. Hyodo, K., Hashimoto, K., Kuchitsu, K., Suzuki, N., Okuno, T., 2017. Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus. Proc. Natl. Acad. Sci. U.S.A. 114, e1282e1290.

Plant Life under Changing Environment

References

347

Ishikawa, T., Shigeoka, S., 2008. Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci. Biotechnol. Biochem. 72, 11431154. Jakubowicz, M., Galganska, H., Nowak, W., Sadowski, J., 2010. Exogenously induced expression of ethylene biosynthesis, ethylene perception, phospholipase D, and Rboh-oxidase genes in broccoli seedlings. J. Exp. Bot. 61, 34753491. Jammes, F., Song, C., Shin, D., Munemasa, S., Takeda, K., Gu, D., et al., 2009. MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 2052020525. Jaspers, P., Kangasja¨rvi, J., 2010. Reactive oxygen species in abiotic stress signaling. Physiol. Plant. 138, 405413. Johnston, E.J., Rylott, E.L., Beynon, E., Lorenz, A., Chechik, V., Bruce, N.C., 2015. Monodehydroascorbate reductase mediates TNT toxicity in plants. Science 349, 10721105. Kangasja¨rvi, S., Lepisto¨, A., Ha¨nnika¨inen, K., Piippo, M., Luomala, E.M., Aro, E.M., et al., 2008. Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem. J. 412, 275285. Karaly-Salama, K.H., Al-Mutawa, M.M., 2009. Glutathione-triggered mitigation in salt-induced alterations in plasmalemma of onion epidermal cells. Int. J. Agric. Biol. 11, 639642. Khan, M.I.R., Iqbal, N., Masood, A., Per, T.S., Khan, N.A., 2013. Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal. Behav. 8, e26374. Available from: https://doi.org/10.4161/psb.26374. Kimura, S., Kaya, H., Kawarazaki, T., Hiraoka, G., Senzaki, E., Michikawa, M., et al., 2012. Protein phosphorylation is a prerequisite for the Ca21-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca21 and reactive oxygen species. Biochim. Biophys. Acta 1823, 398405. Kliebenstein, D.J., Dietrich, R.A., Martin, A.C., Last, R.L., Dangl, J.L., 1990. Regulates salicylic acid induction of copper zinc superoxide dismutase in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 12, 10221026. Ko¨nig, J., Muthuramalingam, M., Dietz, K.J., 2012. Mechanisms and dynamics in the thiol/disulfide redox regulatory network: transmitters, sensors and targets. Curr. Opin. Plant Biol. 15, 261268. Kontos, H.A., 1990. Role of products of univalent reduction of oxygen in hypertensive vascular injury. In: Laragh, J.H., Brenner, B.M. (Eds.), Hypertension: Pathophysiology, Diagnosis and Management. Raven Press Ltd, New York, pp. 667675. Kovtun, Y., Chiu, W.L., Tena, G., Sheen, J., 2000. Functional analysis of oxidative stress activated mitogenactivated protein kinase cascade in plants. Proc. Natl. Acad. Sci. U.S.A. 97, 29402945. Krieger-Liszkay, A., Fufezan, C., Trebst, A., 2008. Singlet oxygen production in photosystem II and related protection mechanism. Photosyn. Res. 98, 551564. Kurusu, T., Kuchitsu, K., Tada, Y., 2015. Plant signaling networks involving Ca21 and Rboh/Nox-mediated ROS production under salinity stress. Front Plant Sci 6, e427. Available from: https://doi.org/10.3389/ fpls.2015.00427. Laloi, C., Apel, K., Danon, A., 2004. Reactive oxygen signalling: the latest news. Curr. Opin. Plant Biol. 7, 323328. Laser, K.D., Lersten, N.R., 1972. Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot. Rev. 38, 425454. Laurindo, F.R., Araujo, T.L., Abraha˜o, T.B., 2014. Nox NADPH oxidases and the endoplasmic reticulum. Antioxid. Redox Signal. 20, 27552775. Lecourieux, D., Mazars, C., Pauly, N., Ranjeva, R., Pugin, A., 2002. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14, 26272641. Lee, S., Park, C.M., 2010. Modulation of reactive oxygen species by salicylic acid in Arabidopsis seed germination under high salinity. Plant Signal. Behav. 5, 15341536. Leisinger, U., Ru¨fenacht, K., Fischer, B., Pesaro, M., Spengler, A., Zehnder, A.J.B., et al., 2001. The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol. Biol. 46, 395408. Leon, A.M., Palma, J.M., Corpas, F.J., Gomez, M., Romero-Puertas, M.C., Chatterjee, D., et al., 2002. Antioxidant enzymes in cultivars of pepper plants with different sensitivity to candium. Plant Physiol. Biochem. 40, 813820.

Plant Life under Changing Environment

348

14. Regulations of reactive oxygen species in plants abiotic stress: an integrated overview

Lindermayr, C., Saalbach, G., Bahnweg, G., Durner, J., 2006. Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. J. Biol. Chem. 281, 17. Lindermayr, C., Sell, S., Mu¨ller, B., Leister, D., Durner, J., 2010. Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22, 28942907. Linster, C.L., Gomez, T.A., Christensen, K.C., Adler, L.N., Young, B.D., Brenner, C., et al., 2007. Arabidopsis VTC2 encodes a GDP-L-galactose phosphorylase, the last unknown enzyme in the Smirnoff-Wheeler pathway to ascorbic acid in plants. J. Biol. Chem. 282, 1887918885. Liu, Y., Burgos, J.S., Deng, Y., Srivastava, R., Howell, S.H., Bassham, D.C., 2012. Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24, 46354651. Liu, Y., Zhang, C., Chen, J., Guo, L., Li, X., Li, W., et al., 2013. Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state. Plant Physiol. Biochem. 64, 9298. Liu, S.L., Luo, Y.M., Yang, R.J., He, C.X., Cheng, Q.S., Tao, J.J., et al., 2015a. High resource-capture and -use efficiency, and effective antioxidant protection contribute to the invasiveness of Alnus formosana plants. Plant Physiol. Biochem. 96, 436447. Liu, S.L., Yang, R.J., Ma, M.D., Dan, F., Zhao, Y., Jiang, P., et al., 2015b. Effects of exogenous NO on the growth, mineral nutrient content, antioxidant system, and ATPase activities of Trifolium repens L. plants under cadmium stress. Acta Physiol. Plant. 37, 172. Available from: https://doi.org/10.1007/s11738-014-1721-7. Liu, S.L., Yang, R.J., Pan, Y.Z., Ma, M.D., Jiang, P., Zhao, Y., et al., 2015c. Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. Ecotoxicol. Environ. Safe 119, 3546. Liu, S.L., Yang, R.J., Pan, Y.Z., Wang, M.H., Hu, J., Wu, M.X., et al., 2015d. Exogenous NO depletes Cd-induced toxicity by eliminating oxidative damage, re-establishing ATPase activity, and maintaining stress-related hormone equilibrium in white clover plants. Environ. Sci. Pollut. Res. 22, 1684316856. Liu, S.L., Yang, R.J., Pan, Y.Z., Ren, B., Chen, Q.B., Li, X., et al., 2016a. Beneficial behavior of nitric oxide in copper-treated medicinal plants. J. Hazard. Mater. 314, 140154. Liu, S.L., Yang, R.J., Ren, B., Wang, M.H., Ma, M.D., 2016b. Differences in photosynthetic capacity, chlorophyll fluorescence, and antioxidant system between invasive Alnus formosana and its native congener in response to different irradiance levels. Botany 94, 10871101. Liu, S.L., Yang, R.J., Tripathi, D.K., Li, X., He, W., Wu, M.X., et al., 2018. The interplay between reactive oxygen and nitrogen species contributes in the regulatory mechanism of the nitro-oxidative stress induced by cadmium in Arabidopsis. J. Hazard. Mater. 344, 10071024. Loughran, P.A., Stolz, D.B., Vodovotz, Y., Watkins, S.C., Simmons, R.L., Billiar, T.R., 2005. Monomeric inducible nitric oxide synthase localizes to peroxisomes in hepatocytes. Proc. Natl. Acad. Sci. U.S.A. 102, 1383713842. Loughran, P.A., Stolz, D.B., Barrick, S.R., Wheeler, D.S., Friedman, P.A., Rachubinski, R.A., et al., 2013. PEX7 and EBP50 target iNOS to the peroxisome in hepatocytes. Nitric Oxide 31, 919. Lumbreras, V., Vilela, B., Irar, S., Sole´, M., Capellades, M., Valls, M., et al., 2010. MAPK phosphatase MKP2 mediates disease responses in Arabidopsis and functionally interacts with MPK3 and MPK6. Plant J. 63, 10171030. Luo, Y., Tang, H., Zhang, Y., 2011. Production of reactive oxygen species and antioxidant metabolism about strawberry leaves to low temperatures. J. Agric. Sci. 3, 8996. Ma, L., Zhang, H., Sun, L., Jiao, Y., Zhang, G., Miao, C., et al., 2012. NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na1/K1 homeostasis in Arabidopsis under salt stress. J. Exp. Bot 63, 305317. Ma, X., Wang, W., Bittner, F., Schmidt, N., Berkey, R., Zhang, L., et al., 2016. Dual and opposing roles of xanthine dehydrogenase in defense-associated reactive oxygen species metabolism in Arabidopsis. Plant Cell 28, 11081126. Mahmood, Q., Ahmad, R., Kwak, S.S., Rashid, A., Anjum, N.A., 2010. Ascorbate and glutathione: protectors of plants in oxidative stress. In: Mahmood, Q., Ahmad, R., Kwak, S.S., Rashid, A., Anjum, N.A. (Eds.), AscorbateGlutathione Pathway and Stress Tolerance in Plants. Springer, Berlin, pp. 209229. Malar, S., Vikram, S.S., Jc Favas, P., Perumal, V., 2016. Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud. 55, 54. Available from: https://doi.org/10.1186/s40529-014-0054-6.

Plant Life under Changing Environment

References

349

Malik, S., Ashraf, M., 2012. Exogenous application of ascorbic acid stimulates growth and photosynthesis of wheat (Triticum aestivum L.) under drought. Soil Environ. 31, 7277. Mata-Pe´rez, C., Sa´nchez-Calvo, B., Padilla, M.N., Begara-Morales, J.C., Luque, F., Melguizo, M., et al., 2016. Nitrofatty acids in plant signaling: nitro-linolenic acid induces the molecular chaperone network in Arabidopsis. Plant Physiol. 170, 686701. Mateo, A., Funck, D., Muhlenbock, P., Kular, B., Mullineaux, P.M., Karpinski, S., 2006. Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J. Exp. Bot. 57, 17951807. Mignolet-Spruyt, L., Xu, E., Ida¨nheimo, N., Hoeberichts, F.A., Mu¨hlenbock, P., Brosche´, M., et al., 2016. Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J. Exp. Bot. 67, 38313844. Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405410. Mittler, R., 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 1519. Mittler, R., 2017. ROS are good. Trends Plant Sci. 22, 1119. Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F., 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490498. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V.B., Vandepoele, K., et al., 2011. ROS signaling: the new wave? Trends Plant Sci. 16, 300309. Mittova, V., Tal, M., Volokita, M., Guy, M., 2003. Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ. 26, 845856. Miura, K., Tada, Y., 2014. Regulation of water, salinity, and cold stress responses by salicylic acid. Front. Plant Sci. 5, e4. Available from: https://doi.org/10.3389/fpls.2014.00004. Møller, I.M., Jensen, P.E., Hansson, A., 2007. Oxidative modifications to cellular components in plants. Annu. Rev. Plant Biol. 58, 459481. Monshausen, G.B., Gilroy, S., 2009. Feeling green: mechanosensing in plants. Trends Cell Biol. 19, 228235. Morgan, P.E., Pattison, D.I., Davies, M.J., 2012. Quantification of hydroxyl radical-derived oxidation products in peptides containing glycine, alanine, valine, and proline. Free Radical. Biol. Med. 52, 328339. Munne´-Bosch, S., Queval, G., Foyer, C.H., 2013. The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol. 161, 519. Mur, L.A.J., Kenton, P., Lloyd, A.J., Ougham, H., Prats, E., 2008. The hypersensitive response: the centenary is upon us but how much do we know? J. Exp. Bot. 59, 501520. Murmu, J., Bush, M.J., DeLong, C., Li, S., Xu, M., Khan, M., et al., 2010. Arabidopsis basic leucine zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for another development. Plant Physiol. 154, 14921504. Murphy, M., 2009. How mitochondria produce reactive oxygen species. Biochem. J. 417, 113. Murphy, M.P., Holmgren, A., Larsson, N.G., Halliwell, B., Chang, C.J., Kalyanaraman, B., et al., 2011. Unraveling the biological roles of reactive oxygen species. Cell Metab. 13, 361366. Nakagami, H., Soukupova, H., Schikora, A., Zarsky, V., Hirt, H., 2006. A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281, 3869738704. Navrot, N., Rouhier, N., Gelhaye, E., Jacquot, J.P., 2007. Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol. Plant 129, 185195. Negi, N.P., Shrivastava, D.C., Sharma, V., Sarin, N.B., 2015. Overexpression of CuZn-SOD from Arachis hypogaea alleviates salinity and drought stress in tobacco. Plant Cell Rep. 34, 11091126. Noctor, G., Paepe, R.D., Foyer, C.H., 2006. Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 12, 125134. Nyathi, Y., Baker, A., 2006. Plant peroxisomes as a source of signalling molecules. Biochim. Biophys. Acta 1763, 14781495. Oikawa, K., Matsunaga, S., Mano, S., Kondo, M., Yamada, K., Hayashi, M., et al., 2015. Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nat. Plants 1, e15035. Available from: https://doi.org/10.1038/nplants.2015.35. Pandey, S., Fartyal, D., Agarwal, A., Shukla, T., James, D., Kaul, T., et al., 2017. Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci. 8, 581. Available from: https://doi.org/10.3389/ fpls.2017.00581.

Plant Life under Changing Environment

350

14. Regulations of reactive oxygen species in plants abiotic stress: an integrated overview

Pastore, D., Stopelli, M.C., Di Fonzo, N., Passarella, S., 1999. The existence of the K1 channel in plant mitochondria. J. Biol. Chem. 274, 2668326690. Pastore, D., Lausa, M.N., Di Fonzo, N., Passarella, S., 2002. Reactive oxygen species inhibit the succinate oxidation-supported generation of membrane potential in wheat mitochondria. FEBS Lett. 516, 1519. Pastore, D., Trono, D., Laus, M.N., Di Fonzo, N., Flagella, Z., 2007. Possible plant mitochondria involvement in cell adaptation to drought stress. A case study: durum wheat mitochondria. J. Exp. Bot. 58, 195210. Pitzschke, A., Hirt, H., 2009. Disentangling the complexity of mitogen-activated protein kinases and reactive oxygen species signaling. Plant Physiol. 149, 606615. Pourrut, B., Perchet, G., Silvestre, J., Cecchi, M., Guiresse, M., Pinelli, E., 2008. Potential role of NADPH-oxidase in early steps of lead-induced oxidative burst in Vicia faba roots. J Plant Physiol. 165, 571579. Rasmusson, A.G., Soole, K.L., Elthon, T.E., 2004. Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu. Rev. Plant Biol. 55, 2339. Rasmusson, A.G., Geisler, D.A., Møller, I.M., 2008. The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8, 4760. Reichler, S.A., Torres, J., Rivera, A.L., Cintolesi, V.A., Clark, G., Roux, S.J., 2009. Intersection of two signalling pathways: extracellular nucleotides regulate pollen germination and pollen tube growth via nitric oxide. J. Exp. Bot. 60, 21292138. Rezende, F., Prior, K.K., Lo¨we, O., Wittig, I., Strecker, V., Moll, F., et al., 2017. Cytochrome P450 enzymes but not NADPH oxidases are the source of the NADPH-dependent lucigenin chemiluminescence in membrane assays. Free Radical Biol. Med. 102, 5766. Rochon, A., Boyle, P., Wignes, T., Fobert, P.R., Despre´s, C., 2006. The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 18, 36703685. Rodriguez, M.C., Petersen, M., Mundy, J., 2010. Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61, 621649. Rodrı´guez-Serrano, M., Romero-Puertas, M.C., Sanz-Ferna´ndez, M., Hu, J., Sandalio, L.M., 2016. Peroxisomes extend peroxules in a fast response to stress via a reactive oxygen species-mediated induction of the peroxin PEX11a. Plant Physiol. 171, 16651674. Rybarczyk-Plonska, A., Hansen, M.K., Wold, A., Hagen, S.F., Borge, G.I.A., Bengtsson, G.B., 2014. Vitamin C in broccoli (Brassica oleracea L. var. italica) flower buds as affected by postharvest light, UV-B irradiation and temperature. Postharvest Biol. Technol. 98, 8289. Sagi, M., Fluhr, R., 2006. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141, 336340. Sandalio, L.M., Rodrı´guez-Serrano, M., Romero-Puertas, M.C., del Rı´o, L.A., 2013. Role of peroxisomes as a source of reactive oxygen species (ROS) signaling molecules. In: del Rı´o, L. (Ed.), Peroxisomes and their Key Role in Cellular Signaling and Metabolism. Subcellular Biochemistry, 69. Springer Nature Press, Dordrecht, Netherlands, pp. 231255. Schlicht, M., Ludwig-Mu¨ller, J., Burbach, C., Volkmann, D., Baluska, F., 2013. Indole-3-butyric acid induces lateral root formation via peroxisome-derived indole-3-acetic acid and nitric oxide. New Phytol. 200, 473482. Schutzendu¨bel, A., Schwanz, P., Teichmann, T., Gross, K., Langenfeld-Heyser, R., Godbold, D.L., et al., 2001. Cadmium-induced changes in antioxidative systems, H2O2 content and differentiation in pine (Pinus sylvestris) roots. Plant Physiol. 127, 887898. Seidel, T., Scholl, S., Krebs, M., Rienmuller, F., Marten, I., Hedrich, R., et al., 2012. Regulation of the V-type ATPase by redox modulation. Biochem. J. 448, 243251. Seminario, A., Song, L., Zulet, A., Nguyen, H.T., Gonza´lez, E.M., Larrainzar, E., 2017. Drought stress causes a reduction in the biosynthesis of ascorbic acid in soybean plants. Front Plant Sci. 8, e1042. Available from: https://doi.org/10.3389/fpls.2017.01042. Seyfferth, C., Tsuda, K., 2014. Salicylic acid signal transduction: the initiation of biosynthesis, perception and transcriptional reprogramming. Front. Plant Sci. 5, 697. Available from: https://doi.org/10.3389/fpls.2014.00697. Shaikhali, J., Heiber, I., Seidel, T., Stro¨her, E., Hiltscher, H., Birkmann, S., et al., 2008. The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes. BMC Plant Biol. 8, e48. Available from: https://doi.org/10.1186/1471-2229-8-48. Sharma, P., Dubey, R.S., 2004. Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci. 167, 541550.

Plant Life under Changing Environment

References

351

Sharma, P., Jha, A.B., Dubey, R.S., Pessarakli, M., 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot. 2012, e217037. Available from: https://doi. org/10.1155/2012/217037. Sinha, A.K., Jaggi, M., Raghuram, B., Tuteja, N., 2011. Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal. Behav. 6, 196203. Son, Y., Cheong, Y., Kim, N., Chung, H., Kang, D.G., Pae, H., 2011. Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways? J. Signal. Transduct. 2011, e792639. Available from: https://doi.org/10.1155/2011/792639. Spiess, G.M., Zolman, B.K., 2013. Peroxisomes as a source of auxin signaling molecules. Subcell. Biochem. 69, 257281. Stevens, R., Page, D., Gouble, B., Garchery, C., Zamir, D., Causse, M., 2008. Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ. 31, 10861096. Suzuki, N., Miller, G., Morales, J., Shulaev, V., Torres, M.A., Mittler, R., 2011. Respiratory burst oxidases: the engines of ROS signaling. Curr. Opin. Plant Biol. 14, 691699. Suzuki, N., Miller, G., Salazar, C., Mondal, H.A., Shulaev, E., Cortes, D.F., et al., 2013. Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell. 25, 35533569. Tada, Y., Spoel, S.H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., et al., 2008. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952956. Takagi, D., Takumi, S., Hashiguchi, M., Sejima, T., Miyake, C., 2016. Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol. 171, 16261634. Takahashi, S., Murata, N., 2008. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 13, 178182. Tama´s, L., Mistrı´k, I., Alemayehu, A., Zelinova´, V., Boˇcova´, B., Huttova´, J., 2015. Salicylic acid alleviates cadmium-induced stress responses through the inhibition of Cd-induced auxin-mediated reactive oxygen species production in barley root tips. J. Plant Physiol. 17, 18. Taylor, N.L., Tan, Y.F., Jacoby, R.P., Millar, A.H., 2009. Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J. Proteomics 72, 367378. Teige, M., Scheikl, E., Eulgem, T., Do´czi, R., Ichimura, K., Shinozaki, K., et al., 2004. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell 15, 141152. Tripathy, B.C., Oelmu¨ller, R., 2012. Reactive oxygen species generation and signaling in plants. Plant Signal. Behav. 7, 16211633. Truman, W., Sreekanta, S., Lu, Y., Bethke, G., Tsuda, K., Katagiri, F., et al., 2013. The CALMODULIN-BINDING PROTEIN60 family includes both negative and positive regulators of plant immunity. Plant Physiol. 163, 17411751. Tseng, M.J., Liu, C.W., Yiu, J.C., 2007. Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol. Biochem. 45, 822833. Turrens, J.F., 2003. Mitochondrial formation of reactive oxygen species. J. Physiol. 552, 335344. Upadhyaya, C.P., Venkatesh, J., Gururani, M.A., Asnin, L., Sharma, K., Ajappala, H., et al., 2011. Transgenic potato overproducing L-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity. Biotechnol. Lett. 33, 22972307. Vaahtera, L., Brosche´, M., Wrzaczek, M., Kangasja¨rvi, J., 2014. Specificity in ROS signaling and transcript signatures. Antioxid. Redox Signal. 21, 14221441. Van Breusegem, F., Bailey-Serres, J., Mittler, R., 2008. Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol. 147, 978984. Voothuluru, P., Sharp, R.E., 2013. Apoplastic hydrogen peroxide in the growth zone of the maize primary root under water stress. I. Increased levels are specific to the apical region of growth maintenance. J. Exp. Bot. 64, 12231233. Wan, D., Li, R., Zou, B., Zhang, X., Cong, J., Wang, R., et al., 2012. Calmodulin-binding protein CBP60g is a positive regulator of both disease resistance and drought tolerance in Arabidopsis. Plant Cell Rep. 31, 12691281.

Plant Life under Changing Environment

352

14. Regulations of reactive oxygen species in plants abiotic stress: an integrated overview

Wang, S., Huang, H., Moll, J., Thauer, R.K., 2010a. NADP1 reduction with reduced ferredoxin and NADP1 reduction with NADH are coupled via an electron-bifurcating enzyme complex in Clostridium kluyveri. J. Bacteriol. 192, 51155123. Wang, Y.C., Qu, G.Z., Li, H.Y., Wu, Y.J., Wang, C., Liu, G.F., et al., 2010b. Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii. Mol. Biol. Rep. 37, 11191124. Wang, Y., Yang, J., Yi, J., 2012. Redox sensing by proteins: oxidative modifications on cysteines and the consequent events. Antioxid. Redox Signal. 16, 649657. Wang, C.H., Zhang, C., Xing, X.H., 2016. Xanthine dehydrogenase: An old enzyme with new knowledge and prospects. Bioengineered 7, 395405. Wang, H., Gui, M., Tian, X., Xin, X., Wang, T., Li, J., 2017. Effects of UV-B on vitamin C, phenolics, flavonoids and their related enzyme activities in mung bean sprouts (Vigna radiata). Int. J. Food Sci. and Technol. 52, 827833. Watanabe, S., Kounosu, Y., Shimada, H., Sakamoto, A., 2014. Arabidopsis xanthine dehydrogenase mutants defective in purine degradation show a compromised protective response to drought and oxidative stress. Plant Biotechnol. Nar 31, 173178. Wei, F., Hu, J., Yang, Y., Hao, Z., Wu, R., Tian, B., et al., 2015. Transgenic Arabidopsis thaliana expressing a wheat oxalate oxidase exhibits hydrogen peroxide related defense response. J. Integr. Agric. 14, 25652573. Wi, S.J., Ji, N.R., Park, K.Y., 2012. Synergistic biosynthesis of biphasic ethylene and reactive oxygen species in response to hemibiotrophic Phytophthora parasitica in tobacco plants. Plant Physiol. 159, 251265. Willekens, H., Langebartels, C., Tire, C., Van Montagu, M., Inze, D., Van Camp, W., 1994. Differential expression of catalase genes in Nicotiana plumbaginifolia (L.). Proc. Natl. Acad. Sci. U.S.A. 91, 1045010454. Wise, R.R., Naylor, R.R., 1987. Chilling-enhanced photooxidation: evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol. 83, 278282. Woyda-Ploszczyca, A.M., Jarmuszkiewicz, W., 2014. Sensitivity of the aldehyde-induced and free fatty acidinduced activities of plant uncoupling protein to GTP is regulated by the ubiquinone reduction level. Plant Physiol. Biochem. 79, 109116. Wrzaczek, M., Brosche´, M., Kangasja¨rvi, J., 2013. ROS signaling loopsproduction, perception, regulation. Curr. Opin. Plant Biol. 16, 575582. Wu, Y., Zhang, D., Chu, J.Y., Boyle, P., Wang, Y., Brindle, I.D., et al., 2012. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 1, 639647. Wu, J., Cheng, Z., Reddie, K., Carroll, K., Hammad, L.A., Karty, J.A., et al., 2013. RegB kinase activity is repressed by oxidative formation of cysteine sulfenic acid. J. Biol. Chem. 288, 47554762. Wu, X., He, J., Chen, J., Yang, S., Zha, D., 2014. Alleviation of exogenous 6-benzyladenine on two genotypes of eggplant (Solanum melongena Mill.) growth under salt stress. Protoplasma 251, 169176. Wu, M.X., Luo, Q., Zhao, Y., Long, Y., Liu, S.L., Pan, Y.Z., 2017. Physiological and biochemical mechanisms preventing Cd toxicity in the new hyperaccumulator Abelmoschus manihot. J. Plant Growth Regul. Available from: https://doi.org/10.1007/s00344-017-9765-8. Xia, X.J., Zhou, Y.H., Shi, K., Zhou, J., Foyer, C.H., Yu, J.Q., 2015. Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J. Exp. Bot. 66, 28392856. Xing, Y., Jia, W., Zhang, J., 2008. AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J. 54, 440451. Xu, J., Zhang, S., 2015. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci. 20, 5664. Xu, J., Li, Y., Wang, Y., Liu, H., Lei, L., Yang, H., et al., 2008. Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J. Biol. Chem. 283, 2699627006. Yamauchi, T., Yoshioka, M., Fukazawa, A., Mori, H., Nishizawa, N.K., Tsutsumi, N., et al., 2017. An NADPH oxidase RBOH functions in rice roots during Lysigenous aerenchyma formation under oxygen-deficient conditions. Plant Cell 29, 775790. Yang, Y., Han, C., Liu, Q., Lin, B., Wang, J., 2008. Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiol. Plant. 30, 433440. Yang, Q.S., Wu, J.H., Li, C.Y., Wei, Y.R., Sheng, O., Hu, C.H., et al., 2012. Quantitative proteomic analysis reveals that antioxidation mechanisms contribute to cold tolerance in plantain (Musa paradisiaca L.; ABB Group) seedlings. Mol. Cell Proteomics 11, 18531869.

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Further reading

353

Yin, L., Wang, S., Eltayeb, A.E., Uddin, M.I., Yamamoto, Y., Tsuji, W., et al., 2010. Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminium stress in transgenic tobacco. Planta 231, 609621. Yun, B.W., Feechan, A., Yin, M., Saidi, N.B., Le, B.T., Yu, M., et al., 2011. S-Nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, 264268. Za´dor, J., Miller, J.A., 2013. Unimolecular dissociation of hydroxypropyl and propoxy radicals. Proc. Combust. Inst. 34, 519526. Zarepour, M., Kaspari, K., Stagge, S., Rethmeier, R., Mendel, R.R., Bittner, F., 2010. Xanthine dehydrogenase AtXDH1 from Arabidopsis thaliana is a potent producer of superoxide anions via its NADH oxidase activity. Plant Mol. Biol. 72, 301310. Zechmann, B., Mu¨ller, M., 2010. Subcellular compartmentation of glutathione in dicotyledonous plants. Protoplasma 246, 1524. Zhao, J., Davis, L.C., Verpoorte, R., 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol. Adv. 23, 283333. Zhu, J.K., 2016. Abiotic stress signaling and responses in plants. Cell 67, 313324. Zou, J.J., Li, X.D., Ratnasekera, D., Wang, C., Liu, W.X., Song, L.F., et al., 2015. Arabidopsis calcium-dependent protein kinase 8 and catalase 3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27, 14451460.

Further reading Koppenol, W.H., 2001. The Haber-Weiss cycle—70 years later. Redox Rep. 6, 229234. Miller, G., Shulaev, V., Mittler, R., 2008. Reactive oxygen signaling and abiotic stress. Physiol. Plant 133, 481489.

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C H A P T E R

15 Plant microbe interactions in plants and stress tolerance Hassan Etesami Faculty of Agricultural Engineering & Technology, Department of Soil Science, Agriculture & Natural Resources Campus, University of Tehran, Tehran, Iran

15.1 Introduction The evolvement of modern agricultural applications has been the consequence of the knowledge obtained from the study of interactions that occur between plants and their associated microorganisms. These interactions have long been of interest for researchers. It has been well known that many plant-associated microbiomes have capacity to confer the promotion of plant growth and enhance resistance against various abiotic stresses (Compant et al., 2010). By interactions within the rhizosphere, plant communities can influence the soil microbes (Berg and Smalla, 2009). Due to being directly affected by the activity of plant root system, rhizosphere environment is more favorable microhabitats for microorganisms compared to nonrhizosphere environment (soil) (Bais et al., 2006). The complexity of the plant microbe interactions in soil makes us understand the detailed mechanisms involved in these reputed selection processes highly difficult for researchers. Microbial root colonization often initiates with the distinction of peculiar compounds in the root exudates by microorganisms. These compounds likely also determine belowground community interactions (Compant et al., 2010). Plants secrete a wide range of organic compounds between 6% and 21% of the carbon fixed (Etesami and Beattie, 2017). These exudates that are used either as nutrients or as signals by microbial populations include different sugars (such as glucose, xylose, fructose, maltose, sucrose, and ribose), amino acids, fatty acids, nucleotides, putrescine, vitamins, and various organic acids (e.g., citric, malic, lactic, succinic, oxalic, and pyruvic acids) (Etesami, 2018a; Etesami and Maheshwari, 2018). The signal molecules can also be used for cross-talk between the plant and microbes (Lugtenberg, 2015). Phytohormones [e.g., indole-3-acetic acid (IAA), jasmonic acid (JA), ethylene, salicylic acid (SA)], volatile compounds, and small molecules produced by microorganisms are directly or indirectly involved in triggering plant immunity

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and regulating the growth and morphogenesis of plants (Ortı´z-Castro et al., 2009). Soil conditions and the amount and composition of root exudates (Dimkpa et al., 2009a), which are important in the specificity of interactions between plant and microbes, influence the type of interaction (e.g., epiphytes, endophytes, symbionts, or pathogens) between plant and its associated microorganisms. Soil factors, which determine survival of microorganisms, plant factors, which determine colonization and compatibility of microorganisms, and microbial factors, which determine the ability of the microorganisms to survive and compete within and on the root, are determinant factors for the community structure of microorganisms (Gaiero et al., 2013). In general, plants select those soil organisms that are successful, competent microorganisms. In other words, plants act as true filters of soil microorganisms, harboring speciesspecific (Acosta-Martı´nez et al., 2008) and cultivar-specific bacterial populations (Manter et al., 2010). In addition, it has been reported that different plant species or cultivars of the same species grown within a single environment harbor the diversity of microbial communities (Berg and Smalla, 2009; Hartmann et al., 2008). Plant-associated microorganisms can be grouped into rhizosphere microorganisms, which reside in vicinity of root, rhizoplane microorganisms, which reside on surface of root, and endophytic microorganisms, which inhabit the interior of tissues and don’t cause harm to the host. The epiphytic microorganisms (living on the surface of plants) are also the microorganisms isolated from rhizoplane (root) and phylloplane (leaves) surfaces of plants (Sturz et al., 2000). There are three basic divisions of microbial interactions based on ecology, namely, neutral, negative, and positive interactions universally exist between microorganisms and plants (Martinez, 2010; Whipps, 2001). A majority of the plant-associated microorganisms establish an innocuous interplay with the host plants indicating no visible effect on the growth and overall physiology of their host plant (Beattie, 2007). These organisms are also known as commensal microorganism. In negative interplay the phytopathogenic microorganisms produce phytotoxic substances such as hydrogen cyanide (HCN) or ethylene, thus adversely influence on the physiology and growth of the plants (Khalid et al., 2004). In contrast to the deleterious microorganisms, some of these microorganisms can boost plant growth and development either directly and indirectly (Etesami and Beattie, 2017; Glick, 2015). It has been known that the mechanisms used by associative microorganisms and endophytic ones to influence the growth and yield of plants are the same (Lugtenberg and Kamilova, 2009). Among the bacteria reintroduced by plant inoculation in a soil containing competitive microorganisms, only about 2% 5% of which were able to exert an advantageous effect on the growth and yield of plants (Etesami et al., 2015a; Paul and Lade, 2014). Bacteria of miscellaneous genera such as Arthrobacter, Azotobacter, Azospirillum, Bacillus, Enterobacter, Pseudomonas, Rhizobium, and Serratia (Etesami and Beattie, 2017; Gray and Smith, 2005), as well as actinobacteria Streptomyces spp. (Dimkpa et al., 2009a) were identified as PGPR (plant growth promoting rhizobacteria). The mechanisms of increasing plant tolerance to nonbiological stresses with the use of beneficial microorganisms can be divided into two categories: (1) strengthening the plant’s defense system against nonliving stresses by reinforcing the antioxidant defense system, increasing the accumulation of protective compounds in the cell, increasing the production of some secondary metabolites, increasing the production of heat shock proteins, and

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adjusting the levels of plant hormones and (2) specific mechanisms for varying the expression levels of stress response genes, such as the HKT1 gene involved in the entry of sodium to the root, improving soil structure and decreasing the absorption of sodium ions, decreasing the mobility of heavy metals by producing siderophores and increasing plant access to nutrients as phosphorus and iron (Yang et al., 2009). In general, some of the known mechanisms by which plant-associated rhizobacteria could be beneficial to the plants include (1) biological nitrogen fixation; (2) generation of essential enzymes involved in diminishing the level of environmental stresses-mediated “stress ethylene” in the root of developing plants such as 1-aminocyclopropane-1carboxylate (ACC) deaminase; (3) the production of some numerous plant growth regulators [e.g., abscisic acid (ABA), gibberellic acid (GA), cytokinins (CKs), and auxin, that is, IAA]; (4) production of siderophores; (5) solubilization and mineralization of micro- and macronutrients, particularly mineral insoluble phosphate (Etesami et al., 2015a; Etesami and Beattie, 2017); (6) the control of plant pathogens by miscellaneous mechanisms such as the production of antibiotic and siderophores (chelation of available Fe in the rhizosphere), induced systemic resistance (ISR), quorum quenching, synthesis of extracellular enzymes hydrolyzing the fungal cell wall, and competition for niches within the rhizosphere (Compant et al., 2010); (7) ameliorating soil structure and bioremediating the contaminated agricultural soils by sequestering toxic heavy metal species and degrading xenobiotic compounds; and (8) improvement of abiotic stresses resistance (Etesami and Beattie, 2017; Glick, 2014; Hayat et al., 2010; Olanrewaju et al., 2017). Since a long time ago, researchers have been fascinated in the use of plant-associated beneficial rhizobacteria to augment the growth and yield of plants (Etesami and Maheshwari, 2018). Nevertheless, the role of the environmental stresses resistant PGPR in handling of nonbiological stresses is acquiring importance in recent years. Augmented incidence of nonbiological stresses has become major cause for stagnation of productivity in principle crops (Etesami and Beattie, 2017; Etesami and Maheshwari, 2018; Grover et al., 2011). In the present time, due to increasing different stresses and their subsequent yield declines in various crops, evolving efficient, low cost, easily adaptable methods for handling the abiotic stress is a major challenge. Changing the crop calendars, resource management practices, developing environmental stress (e.g., drought, salinity, heavy metal toxicity, nutrient deficiency, heat), tolerant varieties, etc. were some of the worldwide researches performed by researchers to develop strategies to cope with nonbiological stresses (Etesami and Maheshwari, 2018; Venkateswarlu and Shanker, 2009). However, most of these technologies are cost-intensive and need to be replaced to appropriate and alternative methods. The ability of plant-associated environmental stresses resistant PGPR in diminishing abiotic stresses in different plants has been shown in recent studies. Due to having some abilities such as their interactions with crop plants, their unique properties of tolerance to extremities, and their potential deployment methods, environmental stresses resistant rhizobacteria play a significant role in stress alleviation in the plants cultivated in stressful agricultural land. Recent overtures in plant microbe interactions research made public that plants are able to mold their rhizosphere and endorhiza (endosphere) microbiome (Berendsen et al., 2012; Etesami and Beattie, 2018; Noori et al., 2018). Under biological and nonbiological stress conditions, plants can require the presence of associated PGPR (stress tolerance) for

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their growth and establishment in miscellaneous ecosystems (Hardoim et al., 2008). For example, it has been proven that transplanting different plant species in the absence of PGPR is notoriously difficult (Leifert et al., 1989), which hints at a role of bacteria in plant growth under stressful conditions. The researches such as studying the interactions among plant, soil, and the different microorganisms are key and open the new possible ways to exploit PGPR for agricultural purposes, spreading knowledge on their interrelationships (Malusa´ et al., 2012). Microbes get benefitted from plants, because of the augmented availability of nutrients, whereas plants can receive benefits from bacterial associates by growth increment or stress reduction (Etesami and Beattie, 2017, 2018). Therefore mutualistic interactions established between microorganisms and their host plants could have appeared due to the clear positive selection exerted on these associations (Thrall et al., 2007). Plants are colonized both by endophytic microorganisms and rhizosphere ones in their natural environment (Etesami and Beattie, 2017; Gray and Smith, 2005). Plants-associated microorganisms, especially beneficial rhizobacteria and rhizofungi, can augment plant performance under stress-affected environments and, therefore, augment yield of plants both directly and indirectly (Dimkpa et al., 2009a). In general, three major groups of microorganisms are considered beneficial to plant nutrition: mycorrhizal fungi (MF) (Jeffries et al., 2003), rhizobacteria (Podile and Kishore, 2006), and nitrogen fixing rhizobia, which are usually not considered as PGPR (Franche et al., 2008). Since there are more than 94 million organisms in a single gram of soil, with most of them being bacteria (90 million) (Glick, 2015); in this review, main focus is on the role of PGPR in modulating the effects of environmental abiotic stresses such as salinity, drought, heavy metal toxicity, and nutritional imbalance. The reader may refer to comprehensive reviews on the role of fungi in increasing the resistance of plants to nonbiological stresses (Chakraborty et al., 2015; Evelin et al., 2009; Hameed et al., 2014; Latef and Miransari, 2014; Porcel et al., 2012; Rapparini and Pen˜uelas, 2014; Singh et al., 2011).

15.2 Salinity stress As a major issue for agriculture, soil salinity induced stress is one of the most substantial nonbiological stresses all over the world, which changes agronomically useful land into unproductive land by about 1% 2% every year in the arid and semiarid zones (Etesami and Maheshwari, 2018). Soil salinization has made almost 7% of the land on earth and 20% of the total arable agricultural land unarable (FAO, 2012). It has been well found that salinity restricts the growth and development of most plants and subsequently diminishes plant yield (Etesami and Beattie, 2018) as well as causes drastic physiological, morphological, and biochemical changes in salinity stressed plants (Etesami and Beattie, 2017; Etesami and Maheshwari, 2018; Gupta and Huang, 2014). Plants under salinity stress usually toil a water shortage that leads to surplus production of reactive oxygen species (ROS) (oxidative stress) (Xie et al., 2015), which can interrupt normal metabolism (Zushi et al., 2009) and result in detriment to the plasma membrane and endomembrane systems (Gill and Tuteja, 2010). Hydroxyl radical, superoxide anion, hydrogen peroxide, and singlet oxygen are some of the most prominent ROS generated under soil salinity mediated stress conditions (Zushi et al., 2009).

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In general, salinity stress decreases the yield of many crops by hindering protein synthesis, plant photosynthesis, and lipid metabolism, decreasing transpiration rate, number of stomata, stomatal size, green pigments, stomatal conduction and plant biomass, and altering in enzymatic activities [such as SOD (superoxide dismutase), CAT (catalase), POD (peroxidase), and ascorbate POD] and osmolyte accumulation [e.g., total free amino acids, proline, glycine betaine, total soluble sugars (TSS)] (Paul and Lade, 2014). Also, the high concentrations of soluble salts and certain ions (Na1 and Cl2) via their high osmotic pressures, toxicity, and associated inadequate ionic distribution result in nutritional imbalance which unfavorably influence the growth of plant by curbing the uptake and translocation of water and balanced absorption of essential nutritional ions (nutritional deficiency) by the roots (Liu et al., 2015; Xie et al., 2015). It has been found that the use of beneficial microorganisms such as salt tolerant PGPR is one of the effective measures for salinity tolerance by most of the agriculture crops (Etesami and Beattie, 2017, 2018; Etesami and Maheshwari, 2018).

15.2.1 Plant growth promoting rhizobacteria and alleviation of salinity stress in plants Plant-associated salinity-resistant rhizobacteria have been known as effective candidates in salinity stress amelioration in plants (Etesami, 2018b; Etesami and Beattie, 2017, 2018; Lugtenberg et al., 2013; Paul and Lade, 2014; Qin et al., 2016; Shrivastava and Kumar, 2015). Apart from developing mechanisms for own stress tolerance (e.g., taking up K1 within their cells and amassing compatible solutes such as polyols and derivatives, amino acids and their derivatives, sugars and derivatives, betaines, and ectoines) (Etesami and Maheshwari, 2018; Lamosa et al., 1998), salinity-resistant beneficial rhizobacteria can also impart some degree of salinity tolerance to salinity-stressed plants, contribute to plants surviving, augment performance in saline habitats, and diminish the extent of poor growth (Dimkpa et al., 2009a). For example, Pseudomonas fluorescens, isolated from date palm rhizosphere in Saharan region (Zerrouk et al., 2016), and Serratia sp., a halophilic bacterium isolated from a salt lake (Singh and Jha, 2016), improved corn (Zea mays L.) and Triticum aestivum L. (wheat) resistance to salinity and increased plant growth, respectively. Various PGPRs genera including Pseudomonas, Bacillus, Flavobacterium, Azospirillum, Chryseobacterium, Achromobneter, Sinorhizobium, Bradyrhizobium, Aeromonas, and Acetobacter have been reported for maintaining the yield of miscellaneous crop plants cultivated in saline soils (Etesami and Beattie, 2018; Etesami and Maheshwari, 2018). A fascinating point about these genera is that these stress resistant-PGPR maintain their PGP (plant growth promoting) characteristics even in the presence of high concentrations of mineral salts. Some of known benefits of PGPR for plants growing in saline soils (Fig. 15.1) are described below. 15.2.1.1 Production of phytohormones PGPRs modulate plant hormone status by releasing exogenous hormones that may contribute to increased salt tolerance (Ilangumaran and Smith, 2017). It has been known that salinity stress decreases root growth (Baluˇska, 2013). Some salinity-resistant PGPR

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FIGURE 15.1 Beneficial traits of salinity and drought-tolerant PGPR toward salinity and drought stress tolerance in plants grown in saline soils. Broken arrows show rhizobacterial components neutralizing salinity and drought stress effects. Salinity and drought-tolerant PGPR increase the K1/Na1 ratio by selectively enhancing K1 uptake and avoiding translocation of toxic Na1 under saline conditions. These bacteria are capable of increasing the antioxidative systems in plants for ROS scavenging such as enzymatic components of SOD, CAT, APX, POD, and GR and nonenzymatic components of cysteine, glutathione, and ascorbic acid. ACC-deaminase-producing PGPR decrease the excessive ethylene production in plants caused by salinity and drought stresses and thereby eliminate the negative effect of ethylene on roots. Production of phytohormones increases the overall growth and also alters root characteristics (i.e., alteration of root proliferation, metabolism, and respiration rate) to facilitate uptake of water and nutrients. Phytohormone IAA also increases the size of aerial parts of the plants. Cytokinin stimulates cell division, cell enlargement, root elongation, shoot growth, and causes stomatal opening. Production of osmoprotectants (i.e., proline, polyamines, glutamate, and total free amino acids) by PGPR also contributes to salinity and drought stress tolerance in PGPR-inoculated plants. Exopolysaccharides (EPS) bind the toxic Na1 and restrict Na1 influx into roots. Soil aggregation due to production of EPS or alteration of RE hydrates the rhizosphere and helps in enhancing uptake of water and nutrients. EPS also increase RAS. VOCs can trigger induction of high affinity K1 transporter (HKT1) in shoots and reduction of HKT1 in roots, limiting Na1 entry into roots and facilitating shoot-to-root Na1 recirculation. These PGPR can increase the uptake/accumulation of plant nutrients by different mechanisms. For more details, see Dutta and Khurana (2015), Kaushal and Wani (2016), Qin et al. (2016). ACC, 1Aminocyclopropane-1-carboxylate; APX, ascorbate peroxidase; CAT, catalase; GR, glutathione reductase; IAA, indole-3-acetic acid; PGPR, plant growth promoting rhizobacteria; POD, peroxidase; RAS, root-adhering soil; RE, root exudates; ROS, reactive oxygen species; SOD, superoxide dismutase; and VOCs, volatile organic compounds.

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synthesize and secrete IAA, which induces root growth and results in a larger coverage root surface and can, therefore, have positive effects on water acquisition (augmented water use efficiency) and nutrient uptake that are expected to diminish the stress effects of salinity in the plant (Etesami and Beattie, 2017; Nabti et al., 2010; Sadeghi et al., 2012; Saravanakumar and Samiyappan, 2007). CK-producing bacteria (i.e., Pseudomonas aurantiaca, Pseudomonas extremorientalis, and Bacillus subtilis) have also diminished the adverse effects of salinity and, consequently, augmented plant growth under salt stress (Arkhipova et al., 2007; Egamberdieva, 2009). There are some reports that PGPRs (i.e., Burkholderia cepacia, Promicromonospora sp. Pseudomonas putida, Arthrobacter protophormiae, B. subtilis, and Acinetobacter calcoaceticus) may contribute to augmented growth of salt-stressed plants via modulating ABA biosynthesis (Barnawal et al., 2017; Bharti et al., 2016; Etesami and Beattie, 2018; Kang et al., 2014b; Yao et al., 2010). 15.2.1.2 Decreased salinity stress induced ethylene production In plants grown under saline soils, IAA-containing PGPR stimulate ACC levels (as a precursor of ethylene), leading to high ethylene concentration that ultimately augments plant damage (Glick, 2014). PGPR such as P. putida, P. fluorescens, Variovorax paradoxus, Enterobacter sp., Arthrobacter sp., Bacillus sp., and Pantoea dispersa have been reported to act as a sink for ACC, hydrolyzing it by ACC deaminase (Etesami et al., 2014b; Glick, 2014; Habib et al., 2016; Nadeem et al., 2009; Sziderics et al., 2007; Wang et al., 2016a; Yan et al., 2014) to ammonia and α-ketobutyrate and thereby lowering the level of stress ethylene generation in salinity stressed plants (Bal et al., 2013; Etesami and Maheshwari, 2018; Glick, 2014). Environmental stresses-resistant PGPR that harbor ACC deaminase activity may facilitate the formation of longer roots and enhance the survival of plant seedlings during miscellaneous biological and nonbiological stresses (Etesami and Maheshwari, 2018; Wang et al., 2000). In general the diminished growth inhibitory ethylene levels by ACC deaminase-active root-associated PGPR (i.e., P. fluorescens and V. paradoxus) may substantially affect the salt tolerance of the crop plants inoculated with PGPR (Ali et al., 2014; Bharti et al., 2014; Etesami and Maheshwari, 2018; Jiang et al., 2012; Lugtenberg and Kamilova, 2009; Nadeem et al., 2009; Siddikee et al., 2010; Wang et al., 2005). 15.2.1.3 Increase in plant nutrients uptake Studies indicate that salinity diminishes the uptake/accumulation of plant nutrients (Etesami, 2018b; Etesami and Beattie, 2018; Etesami and Maheshwari, 2018) including N (Feigin, 1985), P (Sharpley et al., 1992), and K1 in stressed plants (Botella et al., 1997). Salinity-tolerant beneficial rhizobacteria have been proved to be vital for circulation of plant nutrients in the rhizosphere in many ways, thereby diminishing the need for chemical fertilizers (Etesami and Alikhani, 2016; Etesami and Beattie, 2017; Ghorchiani et al., 2018). Apart from fixing N2, many strains of PGPR can affect plant growth directly by solubilizing P from inorganic insoluble phosphates, such as calcium phosphate, phosphate rock, iron phosphate, and alumnium phosphate and K from K-bearing minerals such as mica, muscovite, and biotite feldspar, augmenting nutrient uptake (Etesami and Beattie, 2017; Etesami et al., 2017; Etesami and Maheshwari, 2018; Gundala et al., 2013; Ogut et al., 2010).

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15.2.1.4 Accumulation of osmolytes in plants Overproduction of miscellaneous types of compatible organic solutes such as proline and glycine betaine has been known as one of the most common stress responses in salinity stressed plants (Etesami, 2018b; Serraj and Sinclair, 2002). In addition, plants can diminish the effect of salinity on their growth and yield via retaining water homeostasis and functioning photosynthetic structures. There are many reports showing PGPR such as B. subtilis, Bacillus amyloliquefaciens, Bacillus aquimaris, Azospirillum brasilense, P. dispersa, Rhizobium tropici, and Paenibacillus polymyxa increased plant salinity stress tolerance by contributing to osmolyte accumulation in salinity-stressed crop plants (Casanovas et al., 2003; Chen et al., 2007; del Amor and Cuadra-Crespo, 2012; Nautiyal et al., 2013; Upadhyay and Singh, 2015; Zarea et al., 2012) and regulating water potential and stomatal opening by affecting hydraulic conductivity and transpiration rate (Ilangumaran and Smith, 2017; Marulanda et al., 2010). The compatible solvents can be accumulated to high level by anew synthesis or transported without interference with vital cellular processes (Etesami and Maheshwari, 2018). Via retaining higher leaf water potential during stress, cleansing free radicals and buffering cellular redox potential keeping plants preserved against oxidative stress, and stabilizing subcellular structures (e.g., membranes and proteins), proline accumulation can alleviate salt stress in salt-affected plants (Etesami and Maheshwari, 2018; Kohler et al., 2009). Ecotine (1,4,5,6-tetrahydro-2-methyle-4-pyrimidine carboxylic acid) also acts as powerful osmoprolectant for several bacteria. The ability of various bacterial species of genera Azospirillum, Pseudomonas, Bacillus, Rhizobium, etc. to protect the plants in saline habitat has been reported. Arora et al. (2006) observed salinitymediated accumulation of poly-β-hydroxyl butlyrate in rhizobia, showing its role in cell protection. In addition, enhanced TSS amount of plants under salinity stress is considered as another substantial defense strategy to get over salinity stress. Upadhyay et al. (2012) illustrated that an augmented proline and total soluble sugar in the PGPR-treated wheat plants significantly contributed to their osmotolerance. Correspondingly, rhizobia could augment the growth and yield of plant and adaptation to abiotic stress of leguminous plants by the metabolism of trehalose (Sua´rez et al., 2008). 15.2.1.5 Ion homeostasis in plants Salinity-tolerant beneficial rhizobacteria are able to augment the absorption of K1 ion by interceding the expression of an ion high-affinity K1 transporter (AtHKT1) in plant under salinity stress conditions and, in turn, a higher K1/Na1 ratio that favor salinity tolerance (Etesami and Beattie, 2018; Nadeem et al., 2013; Rojas-Tapias et al., 2012). PGPRmediated bacterial EPS bind cations including Na1 available for plant uptake, thus helping alleviate salt stress in plants (Ashraf et al., 2004). Further, Ashraf et al. (2004) observed that salinity resistant Azospirillum could restrict Na1 influx into roots. Plus, high K1/Na1 ratio was found in salt-stressed corn (Z. mays L.) plants in which selectivity for Na1, K1, and Ca21 was altered in favor of the plant, upon inoculation with salinity-resistant Azospirillum (Hamdia et al., 2004). Plus, Ca21 level is intimately related to expression of osmotic stress responsive genes (Mahajan and Tuteja, 2005; Zhu, 2002), where in K1 plays an important role in osmotic adjustment in plants (Ashraf et al., 2001). VOCs (volatile organic compounds), lipophilic liquids having high vapor pressures, released from PGPR

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such as B. subtilis, Pseudomonas simiae, and Paraburkholderia phytofirmans increased shoot biomass and modulated stress responses in salinity-stressed plants by specific regulations of Na1 homeostasis (decreased Na1 accumulation) by concurrently downregulating expression of HKT1 in roots but up-regulating it in shoots (Zhang et al., 2008; Bailly and Weisskopf, 2012; Ledger et al., 2016; Vaishnav et al., 2015; Wintermans et al., 2016). 15.2.1.6 Induction of antioxidative enzymes Salinity stress leads to formation of ROS in the plants grown under salinity stress conditions (Hichem et al., 2009). Salinity stress-induced ROS cause trauma to proteins, lipids and nucleic acids in plants. Via inducing the plant synthesis of antioxidative enzymes such as CAT, guaicol POD, and SOD, PGPR degrade ROS generated upon salt shock (Mittova et al., 2003). Application of PGPR, such as B. cepacia, Promicromonospora spp., A. calcoaceticus, Bacillus spp., Exiguobacterium oxidotolerans, Pseudomonas pseudoalcaligenes, Bacillus pumilus, B. subtilis, and Arthrobacter, has shown significant increment of plant defense-related enzymes, such as SOD, POD, CAT, polyphenol oxidase, phenylalanineammonia-lyase, phenolics, and lipoxygenase (Jha et al., 2011; Upadhyay et al., 2011; Upadhyay et al., 2012; Chakraborty et al., 2013; Bharti et al., 2014; Damodaran et al., 2014; Etesami, 2018b; Kang et al., 2014a). PGPR-induced antioxidative enzymes are believed to contribute to the salt stress tolerance in plants due to eliminating hydrogen peroxide (H2O2) from salinity-stressed roots (Kim et al., 2005). Detoxification of cellular H2O2 occurred due to involvement of Asada Halliwell scavenging cycle, a substantial element of plant defense mechanism against ROS (Kim et al., 2005). 15.2.1.7 Production of exopolysaccharides (EPS) Exopolysaccharides (EPS) are long chain polysaccharides formed from sugar substitutes. These sugar units are mainly glucose, galactose, and rhamnose in miscellaneous ratios (Etesami and Maheshwari, 2018). Microbial EPS are grouped into two groups of hemopolysaccharides (i.e., cellulose, dextran, and levan) and heteropolysaccharides (i.e., gellan and xanthan) (Welman and Maddox, 2003). In general, polymeric groups of polysaccharides are variable. EPS play an important role in the resistance of bacteria against stresses, including salinity (Sandhya and Ali, 2015). The ability to produce EPS among bacteria is more than fungi and yeasts (Larpin et al., 2002). EPS-producing salinity-resistant PGPR, such as Pseudomonas mendocina, Halomonas variabilis, Planococcus rifietoensis, Enterobacter sp., Bacillus sp., Bacillus amylolequifaciens, Bacillus insolitus, Microbacterium spp., and Pseudomonas syringae, have been shown to importantly augment the volume of soil macropores and the rhizosphere soil aggregation, resulting in augmented water and fertilizer availability to raise from seeds and plants, which in turn are believed to assist plants to better administer the salt shock (Ashraf et al., 2004; Etesami and Beattie, 2018; Tewari and Arora, 2014). The influence of EPS-producing salinity-resistant beneficial rhizobacteria on the aggregation of root-adhering soils (RAS) has been well characterized (Alami et al., 2000; Etesami and Maheshwari, 2018; Kohler et al., 2006; Qurashi and Sabri, 2012; Upadhyay et al., 2011; Yang et al., 2016). PGPR strains that produce EPS bind cations including Na1, and it thus envisaged increase in population density of EPS-producing salinity-resistant rhizobacteria in the root zone, hence reduce the amount of Na1 accessible for plant uptake, which help diminishing salt stress in salt-affected plants (Etesami and

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Maheshwari, 2018; Geddie and Sutherland, 1993). Earlier, Roberson and Firestone (1992) narrated that the EPS of salinity-resistant rhizobacteria possess unique water holding and cementing virtues that also played a vital role in forming and stabilizing soil aggregates and regulating micro- and macronutrients and water flow across plant roots via formation of biofilm. Despite above-mentioned roles, the role of EPS in augmenting plant resistance to salinity stress needs further study in the future (Etesami and Maheshwari, 2018). 15.2.1.8 Induction of systemic tolerance Via initiating signaling pathways, stress-resistant PGPR induce systemic resistance in plants, known as ISR (Egamberdieva and Lugtenberg, 2014), which brings about higher pathogen resistance of the host plants (Van Loon et al., 1998). Induced systemic tolerance (IST) has been also proposed for PGPR-induced physical and chemical changes that result in augmented tolerance to nonbiological stresses (Etesami and Maheshwari, 2018; Sarma et al., 2012). IST to salt stress was also reported in a study with Arabidopsis thaliana (Zhang et al., 2008) by applying B. subtilis GB03. In addition, it has been found that some of the volatiles organic compounds generated by Bacillus-induced IST in plants (Ryu et al., 2004). Plant-associated beneficial rhizobacteria cause upregulation of genes involved in stress tolerance (Kaushal and Wani, 2016b). Via incrementing the expression of salt stress responsive genes such as RAB18 (LEA), RD29A, RD29B regulons of ABRE (ABA-responsive elements), DRE (dehydration responsive element) as well as transcription factor DREbinding proteins (DREB2b) and also by enriching proteins related to energy metabolism and cell division, particularly connected to amino acid metabolism and the tricarboxylic acid cycle (Banaei-Asl et al., 2015; Qin et al., 2016; Etesami and Maheshwari, 2018), plantassociated beneficial rhizobacteria can also augment salt-stressed plant tolerance to salt stress (Kim et al., 2014). Furthermore, PGPR (i.e., B. subtilis) can also diminish the absorption of immoderate amount of Na1 by the roots of plants by downregulating expression of the high-affinity K1 transporter (HKT1) in the roots of salinity-stressed crop plants (Etesami and Maheshwari, 2018; Qin et al., 2016; Zhang et al., 2008). In addition, these salinity-resistant beneficial rhizobacteria simplify shoot-to-root Na1 recirculation by activating the induction of HKT1 in shoots (Zhang et al., 2008). PGPR (such as A. brasilense, Pantoea agglomerans, and Bacillus megaterium) can also help plants to diminish their cell water potential to carry on to take up water from saline soils (Qin et al., 2016) by augmenting the expression of genes (e.g., PIP2, ZmPIP1-1, and HvPIP2-1) involved in generating aquaporins (augmented root hydraulic conductance) (Etesami, 2018b; Etesami and Maheshwari, 2018). Aquaporins are water channel proteins present in the intracellular membranes and plasma of plant cells, which help to cause the transfer of water into the plant (Marulanda et al., 2010; Zawoznik et al., 2011; Moshelion et al., 2015; Gond et al., 2015).

15.3 Drought stress Drought is one of the major nonbiological stresses that antagonistically affect growth and productivity in a majority of cultivated agricultural crops, specifically in arid and semiarid regions (Naveed et al., 2014; Bodner et al., 2015; Etesami and Maheshwari, 2018).

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It is expected that water-deficit stress along with climate change, which leads to more drastic and frequent droughts, would cause critical plant growth problems for more than 50% of the arable agricultural lands by 2050 (Vinocur and Altman 2005; Etesami and Beattie, 2017; Etesami and Maheshwari, 2018). By influencing water relations, photosynthetic assimilation, and uptake of micro- and macronutrients (Heffernan, 2013), waterdeficit stress results in disadvantageous effects on plant growth and metabolic processes in major field grown crops (Osakabe et al., 2014; Etesami and Maheshwari, 2018). ROS such as superoxide radical (O22), H2O2, and hydroxyl radicals (OH) cause lipid peroxidation and succeeding detriment to proteins, DNA, and lipids (Sgherri et al., 2000; Pompelli et al., 2010; Etesami and Maheshwari, 2018) produced during drought (Vardharajula et al., 2011). In addition, water-deficit stress also affects the absorption and translocation of essential micro- and macronutrients by plants and causes oxidative stress in plants (Anjum et al., 2011; Etesami and Beattie, 2017). The lack of water in the plant leads to cellular plasmolysis and closure of the stomata (in order to prevent evapotranspiration), thereby stopping photosynthesis and increasing photorespiration, while the amount of ethylene also increases and as a result, plant growth decreases (Etesami and Maheshwari, 2018).

15.3.1 Plant growth promoting rhizobacteria and alleviation of drought stress Several drought-resistant beneficial rhizobacteria are reported to induce water-deficit stress tolerance in plants (Saravanakumar and Samiyappan, 2007; Vardharajula et al., 2011; Wang et al., 2012; Kavamura et al., 2013; Etesami and Beattie, 2017; Etesami and Maheshwari, 2018). EPS-producing drought-resistant beneficial rhizobacteria improved survival of the drought-stressed plants from the drought stress (Etesami and Beattie, 2017; Etesami and Maheshwari, 2018). Mechanisms of drought resistance in plants mediated by drought-resistant beneficial rhizobacteria, by drawing out of the so-called rhizobacteriainduced drought endurance and resilience process, involve various physiological and biochemical alterations (Kaushal and Wani, 2016a; Etesami and Beattie, 2017; Etesami and Maheshwari, 2018). In principle, analogous mechanisms of action have been seen in plantassociated beneficial rhizobacteria-induced tolerance of salinity and drought (Fig. 15.1) described in the following subsections. 15.3.1.1 Modifications in phytohormonal content Under water-deficit stress, drought-resistant beneficial rhizobacteria augment plant tolerance to drought by modification of phytohormones such as IAA, GA, CK, ethylene, and ABA (Kavamura et al., 2013; Kaushal and Wani, 2016a; Etesami and Maheshwari, 2018). For example, IAA production by PGPRs (i.e., Pseudomonas chlororaphis, Azospirillum, Bacillus thuringiensis, Acinetobacter, and Pseudomonas) causes changes in root system architecture by augmenting the number of root tips and the root surface area, thus augmenting water and micro- and macronutrients acquisition, which help plants to get over drought stress (Egamberdieva and Kucharova, 2009; Marulanda et al., 2009; Egamberdieva, 2012; Pereyra et al., 2012; Naveed et al., 2014; Timmusk et al., 2014; Rolli et al., 2015; Etesami and Maheshwari, 2018). The role of gibberellin-producing bacteria such as Azospirillum

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lipoferum, B. cepacia, Promicromonospora spp., P. putida, and A. calcoaceticus has been shown to augment the resistance of various plants to drought (Cohen et al., 2009; Kang et al., 2014a,b). CK-producing PGPR (e.g., B. subtilis) have been able to augment the resistance of the plant to drought stress some extent through various mechanisms such as stimulating cell division, cell enlargement, shoot growth, causing stomatal opening and reducing the root to shoot ratio (Arkhipova et al., 2007; Liu et al., 2013; Noori et al., 2018; Etesami and Beattie, 2018). Other plant hormones such as JA and SA can protect plants from the damage caused by oxidative stresses that some bacteria alter the amount of these hormones in the plant under stress (Iqbal and Ashraf, 2010; Kaushal and Wani, 2016a). 15.3.1.2 Decreased stress-induced ethylene production Ethylene biosynthesis increases during water-deficit stress that leads to diminished root and shoots growth (Glick, 2014; Etesami and Maheshwari, 2018). Research has shown that ACC deaminase-possessing beneficial rhizobacteria can cleave the plant ethylene precursor ACC to ammonia and α-ketobutyrate, thereby diminishing stress ethylene level (Glick, 2014). The detrimental effect of “stress ethylene” is abated by the removal of ACC, thus diminishing plant drought stress and inducing longer roots, which results in an augmented uptake of more water from deep soil under water-deficit stress conditions (Glick, 2014; Lim and Kim, 2013; Etesami and Maheshwari, 2018). Some bacteria, such as Achromobacter piechaudii, Bacillus licheniformis, V. paradoxus, Pseudomonas spp., Burkholderia phytofirmans, and Enterobacter spp., have been reported to increase the plant’s resistance to drought through the production of this enzyme (Mayak et al., 2004; Zahir et al., 2008; Belimov et al., 2009; Lim and Kim, 2013; Naveed et al., 2014). 15.3.1.3 Induced plant synthesis of antioxidative enzymes Equipped with antioxidant defense systems constituting both enzymatic and nonenzymatic components, plants act in concert to diminishing the oxidative trauma outcropping during water-deficit stress via scavenging ROS (Miller et al., 2010; Etesami and Maheshwari, 2018). Studies have showed that PGPRs (i.e., Bacillus spp., B. thuringiensis, and Pseudomonas aeruginosa) appended plant defense enzymes such as CAT, POD, SOD, or phenolic compounds to diminish the oxidative damage elicited by water-deficit stress (Vardharajula et al., 2011; Armada et al., 2014; Naseem and Bano, 2014; Naveed et al., 2014; Sarma and Saikia, 2014; Timmusk et al., 2014; Ortiz et al., 2015; Etesami and Maheshwari, 2018). 15.3.1.4 Osmolytes (compatible solutes) accumulation To alleviate their cell turgidity losses, plants have a greater necessity to adjust osmotically under water-deficit conditions. It has been well known that the one of the most frequent acclimatization responses observed in water deficit-affected plants is the accumulation of osmolytes (naturally occurring organic compounds affecting osmosis) such as glycine betaine, proline, and trehalose (Chen and Murata, 2008; Rodrı´guez-Salazar et al., 2009; Etesami and Maheshwari, 2018). In general, drought-resistant beneficial rhizobacteria such as A. brasilense, Bacillus spp., and B. thuringiensis exudate osmolytes such as proline, glycine betaine, trehalose, and soluble sugars in response to water-deficit stress, which operate in a synergistic manner with plant-generated osmolytes and motivate plant

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growth (Rodrı´guez-Salazar et al., 2009; Sandhya et al., 2010; Vardharajula et al., 2011; Cohen et al., 2015; Ortiz et al., 2015; Etesami and Maheshwari, 2018). 15.3.1.5 Generation of exopolysaccharides (EPS) Exopolysaccharides (EPS) are the hydrated compounds with 97% water in a polymer matrix that can augment plant growth and development and ensure plant survival under water-deficit stress (Etesami and Maheshwari, 2018; Nocker et al., 2012; Vu et al., 2009). Via augmenting aggregate stability and RAS/root tissue ratio and enhancing microaggregates, EPS produced by PGPR such as P. agglomerans, Rhizobium spp., P. putida, Bacillus spp., Acinetobacter, and Pseudomonas spp. can help winter plant desiccation and increase the uptake of water and nutrients from rhizosphere soil (Amellal et al., 1998; Alami et al., 2000; Sandhya et al., 2009; Vardharajula et al., 2011; Naseem and Bano, 2014; Rolli et al., 2015; Etesami and Maheshwari, 2018). Since EPS possess unique water-preserving attributes, they can lead to stabilization of soil aggregates and water regulation via drought stressed-plant roots (Roberson and Firestone, 1992; Etesami and Maheshwari, 2018). There are many studies showing augmented EPS production by PGPR during water-deficit conditions as compared to well-watered conditions (Awad et al., 2012; Martı´nez-Gil et al., 2014; Naseem and Bano, 2014; Dutta and Khurana, 2015; Etesami and Maheshwari, 2018).

15.4 Heavy metal toxicity stress Heavy metals, with specific weight more than 5.0 gcm–3, are universally categorized in three classes: (1) toxicant metals such as mercury (Hg), chromium (Cr), lead (Pb), zinc (Zn), cupper (Cu), nickel (Ni), cadmium (Cd), arsenic (As), cobalt (Co), and tin (Sn); (2) valuable metals such as palladium (Pd), platinum (Pt), silver (Ag), gold (Au), and ruthenium (Ru); and (3) radionuclides such as uranium (U), thorium (Th), radium (Ra), and americium (Am) (Bishop and Bishop, 2000). In the current era, heavy-metal pollution is rapidly raising and causing environmental problems. Origin of this pollution may be from anthropogenic and natural sources. Anthropogenic sources (resources originated from human activities) of heavy metals can refer to activities related to mining, industrial emissions, application of sewage sludge to agricultural land, disposal or discharge of municipal and industrial wastes, and fertilizer and pesticide use. Weathering of soil parent material, mineral dissociation, and atmospheric deposition are some of the natural sources of entering heavy metals to environment. These are the sources of jeopardous impacts on both ecological and human health (Bibi et al., 2008; Nagajyoti et al., 2010; Kamran et al., 2014). Since the removal of heavy metals from the environment is difficult, the toxicity of these metals to miscellaneous environments is of great importance for natural science scientists (Etesami, 2018a) because these metals are not degraded chemically or biologically and are finally indestructible, and hence, their toxic effects are prolonged in the environment (Etesami, 2018a; Ahemad, 2012). Albeit some of the heavy metals are needed by organisms at low concentration and essential for their miscellaneous metabolic activities (Noll, 2003), the augmented concentration of such metals more than threshold levels in soils unfavorably affects the composition of microbial communities (microbial diversity and community structure), including plant-associated beneficial bacteria both quantitatively and

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qualitatively (Ahemad, 2012). Excessive heavy metals also exert an unfavorable impact on plant growth, biomass, and photosynthesis (Nagajyoti et al., 2010; Ali et al., 2015; Etesami and Maheshwari, 2018). Toxic heavy metals interfere with the uptake and dissemination of essential micro- and macronutrients in plant causing deficiencies and nutrient imbalance (Sharma and Archana, 2016; Etesami, 2018a). In addition, heavy metals are largely aggregated in soil and are transferred to food chain via plants grown on the soils polluted to heavy metals (Adrees et al., 2015; Etesami, 2018a). Previous studies showed that heavy metal resistant beneficial rhizobacteria could diminish toxic metals bioavailability and their absorption by plant and eventually lead to safe food production (Etesami, 2018a; Etesami and Maheshwari, 2018).

15.4.1 Plant growth promoting rhizobacteria and alleviation of heavy metals toxicity stress in plants Nowadays, heavy metal resistant PGPR also boost plant growth and development in heavy metal polluted agricultural land (Etesami, 2018a; Etesami and Maheshwari, 2018). The PGPR have been prosperously implicated in boosting plant growth and concurrently diminishing the degree of toxicity or detriment to plants exposed to stress generated by different heavy metals in agricultural land (Ma et al., 2011; Ahemad, 2014; Wang et al., 2016b; Etesami, 2018a; Etesami and Maheshwari, 2018). Metal-resistant beneficial rhizobacteria generate plant-growth regulators, mineral solubilizers, phytohormones, and various secondary metabolites, which induce the plant growth and development and augment plant tolerance against various abiotic stresses, including heavy metal induced stress (Ahemad, 2012; He et al., 2013; Rajkumar et al., 2013; Etesami, 2018a; Etesami and Maheshwari, 2018). Moreover, PGPR exhibited the decrease in metal toxicity toward promoting plant-growth when used as inoculants (Rajkumar et al., 2010b; Sessitsch et al., 2013; Etesami, 2018a). Miscellaneous mechanisms are employed by heavy metal resistant beneficial rhizobacteria to augment plant growth (Fig. 15.2), many of which lead to mitigating heavy-metal toxicity (Tank and Saraf, 2010; Ahemad, 2012; Glick, 2012; Sharma and Archana, 2016; Etesami, 2018a; Etesami and Maheshwari, 2018). 15.4.1.1 Generation of siderophores Siderophores, high-affinity iron (Fe31) chelating compounds, can mitigate heavy metal induced stress in plant by providing nutrients exclusively iron to heavy metal stressed plants, decreasing free radical formation around plant roots and patronizing microbial phytohormones from metal-mediated oxidative detriment by means of chelation reaction (Rajkumar et al., 2010a; Złoch et al., 2016; Etesami, 2018a). Metal-resistant rhizobacteria with ability to produce various siderophores play an important role in the successful survival and growth of plants in soils contaminated to heavy metals by diminishing metal toxicity and securing nutrients for stressed plants (Etesami, 2018a; Etesami and Maheshwari, 2018). The bacterial siderophores can bind metals other than iron (Rajkumar et al., 2010a), which may be the reason why metal-resistant rhizobacteria can outlive in the mine tailing soil polluted by multi heavy metals (Yu et al., 2014). Following inoculation of plants with siderophores-generating metal-resistant PGPR, it was found that

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FIGURE 15.2 Beneficial traits of heavy metal tolerant PGPR toward heavy metal toxicity stress tolerance in plants grown in heavy metal contaminated soils. Broken arrows show rhizobacterial components neutralizing heavy metal toxicity stress effects. Heavy metal tolerant PGPR are capable of increasing the antioxidative systems in plants for ROS scavenging such as enzymatic components of SOD, CAT, APX, POD, and GR and nonenzymatic components of cysteine, glutathione, and ascorbic acid. ACC-deaminase-producing PGPR decrease the excessive ethylene production in plants caused by heavy metal toxicity stress and thereby eliminate the negative effect of ethylene on roots. Production of phytohormones increases the overall growth and also alters root characteristics (i.e., alteration of root proliferation, metabolism, and respiration rate) to facilitate uptake of nutrients. Phytohormone IAA also increases the size of aerial parts of the plants. EPS strongly bind potentially toxic trace elements and ensnare precipitated metal oxides and sulfides, resulting in forming organic metal complexes and subsequently enhancing heavy metal resistance in the plants grown in soils contaminated to heavy metals. Organic acids (i.e., succinic acids, gluconic acid, citric acid, and oxalic acid) have affinity to form complexes with heavy metals. These organic acids can detoxify metal ions and decrease the uptake of these metals by the chelation of metal ions (e.g., metaloxalate crystal formation). Bacterial surfactants can bind preferentially to toxic metals with strong affinity, aid in metal removal from soil, and reduce the plant’s access to these metals. Siderophores produced by PGPR can bind heavy metals other than iron, and by doing so, they can probably prevent plant from absorbing heavy metals (e.g., by formation of heavy metal siderophore complex unavailable for plant). Siderophores-producing PGPR do not reduce iron absorption in the presence of other metals by increasing the concentration of Fe, although they are the same membrane transporters for Fe and some heavy metals. Fe wins in this competition due to siderophore-mediated high concentration and availability. For more details, see Etesami (2018a). ACC, 1-Aminocyclopropane-1-carboxylate; APX, ascorbate peroxidase; CAT, catalase; GR, glutathione reductase; IAA, indole-3-acetic acid; PGPR, plant growth promoting rhizobacteria; POD, peroxidase; ROS, reactive oxygen species; and SOD, superoxide dismutase.

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ameliorating the iron availability would result in diminished uptake of heavy metals, thus conferring heavy metals tolerance, as well as betterment of plant growth (Ma et al., 2011; Wu et al., 2012; Etesami, 2018a; Etesami and Maheshwari, 2018). 15.4.1.2 Synthesizing 1-aminocyclopropane-1-carboxylate deaminase Among PGP traits of PGPR, ACC deaminase activity is known as one of the most greatly accepted mechanisms of PGPR under heavy-metal stress (Sessitsch et al., 2013; Etesami, 2018a). This enzyme diminishes growth inhibitory levels of ethylene produced in plants exposed to heavy metal induced stress (stress ethylene). In addition, ACC deaminase may promote root growth (Sessitsch et al., 2013; Glick, 2014). In many plant species, abiotic stress caused by heavy metals has increased stress-ethylene biosynthesis (Chmielowska-Ba˛k et al., 2014; Etesami and Maheshwari, 2018). Surplus production of ethylene results in diminishing root elongation (Sun and Guo, 2013; Etesami and Maheshwari, 2018). PGPR possessing ACC deaminase hydrolyze ACC, thereby decreasing plant ethylene levels, and lead to the enhancement of plant’s ability to grow under heavy metal polluted soil (Safronova et al., 2006; Etesami, 2018a). Since ethylene is envisaged as a nexus in heavy metal mediated accumulation of H2O2 and induction of apoptosis (Chmielowska-Ba˛k et al., 2014), diminished ethylene by ACC deaminase producing heavy metal resistant rhizobacteria help to mitigate the heavy metals toxicity and confer tolerance to metal-stressed plants. 15.4.1.3 Phosphate solubilization By binding heavy metals to the cell wall fraction of microorganisms and forming heavy metal P complexes, P plays important roles in decreasing heavy metal absorption and translocation by the plants grown under heavy-metal stress conditions (Chatterjee et al., 2009; Qiu et al., 2011; Etesami and Maheshwari, 2018). Several PGPR dissolve mineral phosphate complexes such as Ca P, Fe P, and Al P found in P-deficient soils (Gyaneshwar et al., 2002; Etesami, 2018a; Etesami and Maheshwari, 2018). The PGPR with the positive ability in solubilizing phosphate, so-called phosphate-solubilizing bacteria (PSB), increase the P availability to plants. Application of these bacteria (PSB) in heavy metal contaminated soils rapidly immobilizes heavy metals (Park et al., 2010) via sorption of metals to EPS polymers (formation of metal EPS complex) (Susilowati and Syekhfani, 2014; Etesami, 2018a; Etesami and Maheshwari, 2018). According to findings of Cao et al. (2008), solubilized P led to Pb immobilization via formation of Pb5(PO4)3 (pyromorphite). On the other hand, PSB augment Cd21 immobilization by the dissolution of P and next precipitation and formation of insoluble Cd phosphate (Cd3(PO4)2) (Sharma and Archana, 2016). Since exudation of organic acids is responsible for mineral phosphate solubilization, organic P mineralization (Patel et al., 2010; Etesami, 2018a; Etesami and Maheshwari, 2018), and zinc solubilization, heavy metal resistant beneficial rhizobacteria mediated secretion of organic acids showed effective effects on plants subjected to heavy metals stress because of combination of environmental factors (Etesami, 2018a).

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15.4.1.4 Production of organic acids Assorted metal resistant rhizospheric bacteria are able to produce low molecular weight organic acids such as gluconic acid, citric acid, oxalic acid, and succinic acid (Archana et al., 2012; Etesami, 2018a). It has been known that organic acids have a high affinity to form complexes with various heavy metals (Kavita et al., 2008; Etesami, 2018a). It has been reported that the one of the most important modes of metal ion detoxification by heavy metal resistant beneficial rhizobacteria is the chelation of metal ions by these organic acids (Etesami and Maheshwari, 2018). Upon exposure to heavy metals, plants along with their associated PGPR secrete organic compounds including disparate organic acids (Matusik et al., 2008; Etesami, 2018a; Etesami and Maheshwari, 2018). Owing to the formation of metal-oxalate crystals, organic acids (e.g., oxalic acid) generated by heavy metal resistant beneficial rhizobacteria can provide both advantages in the acquisition of nutrients for plants and tolerance to toxic heavy metals (Etesami, 2018a; Gadd, 2010). The advantageous effect of organic acids was reverberated by reversal of biochemical parameters such as SOD and POD upregulation under heavy metals stress. In previous studies (Kavita et al., 2008; Etesami, 2018a), it has been reported that the supplementation of organic acids such as citrate and oxalate could diminish Cd toxicity to plants and regulate the antioxidant enzyme response revealed by Cd-contaminated soil grown plants. 15.4.1.5 Biosurfactant production It has been reported heavy metal resistant rhizobacteria augment heavy metals tolerance and aid in metal removal from soil by generating the surface-active amphiphilic biomolecules (i.e., glycolipids, fatty acids, phospholipids, neutral lipids, and lipopeptides), which are also called biosurfactants (Pacwa-Płociniczak et al., 2011; Etesami, 2018a). It should be noted that microbial surfactants are preferentially bound to toxic heavy metals with strong affinity in comparison with the normal soil metal cations (Braud et al., 2006; Etesami, 2018a). 15.4.1.6 Generation of phytohormones By producing phytohormones (auxins, CKs and gibberellins, etc.), plant-associated beneficial rhizobacteria motivate plant growth under normal conditions as well as under stressful conditions (Etesami and Maheshwari, 2018). One of the most important phytohormones produced by PGPR is IAA (Glick, 2014; Etesami et al., 2015b). By elevating plant growth in soils polluted to metal heavy metals, simplifying conformity and tolerance to metals in heavy metal stressed plants (via inducing physiological alterations), and promoting uptake of micro- and macronutrients and metals (by augmenting plant roots), IAA-producing heavy metal resistant rhizobacteria can also diminish the heavy metals induced stress in stressed plants (Chatterjee et al., 2009; Bhattacharyya and Jha, 2012; Sessitsch et al., 2013; Etesami, 2018a; Etesami and Maheshwari, 2018). For example, in a previous study (Chmielowska-Ba˛k et al., 2014), auxins alleviated Cd toxicity in Cdstressed plants by diminishing Cd sorption and translocation or stimulating antioxidants and antioxidant-related enzymes.

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15.4.1.7 Betterment in the uptake of micro- and macronutrients Toxic heavy metals inure deficiencies and nutrient imbalance in the plants grown in soils polluted with heavy metals via interfering with the uptake and distribution of microand macronutrients in heavy metal stressed plants (Barcelo´ and Poschenrieder, 1990; Etesami and Maheshwari, 2018). For example, due to having almost similar chemical attributes to heavy metals such as Ca21, Mg21, Zn21, and Fe21, cadmium (Cd21) competes with these mineral nutrients and leads to mineral deficiency in the plants grown in the agricultural land contaminated to Cd (Barcelo´ and Poschenrieder, 1990; Etesami, 2018a). Via ameliorating the uptake of micro- and macronutrients (i.e., Mg, P, Ca, N, S, Fe, Zn, and Mn) by plants (Saravanan et al., 2011; Guo and Chi, 2014; Sharma and Archana, 2016; Etesami, 2018a; Etesami and Maheshwari, 2018), heavy metal tolerant rhizobacteria are capable of diminishing heavy-metal toxicity to some extent to the plants and augmenting plant resistance to heavy metal induced stress (Gomes et al., 2012; Etesami, 2018a; Etesami and Maheshwari, 2018). 15.4.1.8 Production of exopolymers It has been reported that heavy metal resistant PGPR can augment the plant resistance to heavy metal toxicity by generating EPS (i.e., polysaccharides, mucopolysaccharides, humic substances, and proteins), which strongly bind heavy metals and entrap precipitated metal sulfides and oxides (formation of EPS metal complexes) (Rajkumar et al., 2010a; Xu et al., 2012; Etesami, 2018a). According to findings of Xu et al. (2012), Cd-resistant P. putida could transform the bioavailable Cd21 into organic species by EPS (formation of Cd21 EPS complex). In a previous study, it was found that bacterial exopolysaccharides can be linked to heavy metals (i.e., Cd) due to the presence of their functional groups such as carboxyl and phosphate groups (Wei et al., 2011). 15.4.1.9 Diminished uptake of heavy metals The low bioavailability and high bioavailability of heavy metals in heavy metal contaminated soils diminish and augment their uptake by stressed plants, respectively (Braud et al., 2006; Etesami, 2018a). Therefore in order to prevent the entry of these metals into plants the most important step is to diminish the bioavailability of these elements (the conversion of bioavailable heavy metals into inert species) in the plant growth environment (Etesami, 2018a). It has been known that, by altering the speciation from bioavailable forms to the nonbioavailable forms of heavy metals in soils, heavy metal resistant PGPR can protect the stressed plants from the phytotoxicity of excessive metal metals (Zou et al., 2007; Etesami, 2018a). Some of the most important mechanisms by which heavy metal resistant PGPR could diminish the bioavailability of heavy metals in the rhizosphere, thereby prevent their entry into the plant tissues include (Etesami, 2018a): (1) biotransformation of toxic soluble heavy metals into nontoxic insoluble forms. Precipitation of heavy metals with microbially produced anions such as sulfides and phosphates is a biotransformation of toxic soluble heavy metals (Siripornadulsil and Siripornadulsil, 2013); (2) acidification and oxidation reduction (Ma et al., 2011; Ahemad, 2012; Etesami, 2018a); (3) complexation by producing numerous organic substances (Saravanan et al., 2007; Xu et al., 2012) and by the production of secondary metabolites

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such as exopolysaccharides and siderophores and substances with functional groups, that is, sulfhydryl, carboxyl, hydroxyl, sulfonate, amine, and amides; (4) biosorption or sequestration of heavy metals (Etesami, 2018a; Sessitsch et al., 2013) via binding and accumulating selected metal ions in their surface, in their exopolysacharide layer, in extracellular capsules, and on cell wall of bacteria (Madhaiyan et al., 2007; Ahemad and Kibret, 2013; Marques et al., 2013); and (5) bioaccumulation of heavy metals within their cells (Kumar et al., 2011). 15.4.1.10 Heavy metals resistant genes induction Microbe-mediated induction of abiotic stress responses (known as IST) in stressed plants is has been well proven (Yang et al., 2009). For example, via mechanisms such as ethylene production and stress proteins (Sziderics et al., 2007; Dimkpa et al., 2009b; Sessitsch et al., 2013; Etesami, 2018a), heavy metal resistant beneficial rhizo-bacteria can induce heavy metal resistant genes and the expression of more general stress response in plants under assorted environmental stresses including toxicity of heavy metals (heavy metal contaminated soils) (Etesami, 2018a; Etesami and Maheshwari, 2018).

15.5 Mineral nutritional imbalance stress Mineral nutritional imbalance (nutritional deficiency and excess) hampers the growth and development of crop plants (Etesami and Maheshwari, 2018; Paul and Lade, 2014). Some of the unfavorable aftereffects of nutritional deficiency and excess are soil salinization, competitive ions absorption, transport or separation within the plant, which may occur due to physiological deactivation of a given nutrient leading to an increment in the plant’s interior demand for characteristic essential nutrient (Grieve and Grattan, 1999; Etesami and Beattie, 2017; Etesami and Maheshwari, 2018). Due to the nutrients being bound in soils to inorganic and organic soil ingredients and being presented as insoluble precipitates, a large quantity of these nutrients is not available for absorption by stressed plants. It is known that the most feasible and easiest way of combating stresses is to administer the plants nutrient (Abbas et al., 2015; Etesami and Beattie, 2017; Etesami, 2018b). Research has disclosed that a good nutrient handling can help plants to greatly affect the ability of plants to adapt to damaging environmental conditions and especially to nonbiological stress factors (Etesami and Maheshwari, 2018). For example, it has been reported that the defect of the mineral nutrition status of plants exacerbated the damaging effects of nonbiological stresses on the plants grown under stress conditions (Baligar et al., 2001; Khoshgoftarmanesh et al., 2010; Etesami and Maheshwari, 2018). Many previously published studies revealed that plants exposed to biological and nonbiological stresses require extra supplies of mineral nutrients to diminish the detrimental effects of stress (Endris and Mohammad, 2007; Heidari and Jamshid, 2010; Etesami and Maheshwari, 2018). In general, by influencing plant nutritional status or water uptake and via toxic effects on plant cells, imbalances in the mineral content of soils (nutritional deficiency and excess) can affect stressed-plant fitness.

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15.5.1 Plant growth promoting rhizobacteria and the availability of nutrients The low availability of micro- and macronutrients can be an important barrier to plant growth and development in many agricultural lands in the world, especially tropical regions where soils are poor in terms of nutrients (Etesami and Beattie, 2017). In previous studies, augmented ability of crop plants to survive and produce yield in micro- and macronutrients poor agricultural land by plant-associated microorganisms has been well proven (Paul and Nair, 2008; Glick, 2012, 2015; Etesami and Beattie, 2018). Beneficial rhizosphere microorganisms can, by changing the solubility of the nutrients that their concentration in the soil solution is very low (i.e., P and Fe) and even changing the conditions of their absorption by plants, augment the availability of the nutrients for plants grown in nutrient-deficient conditions (Etesami and Beattie, 2017; Etesami and Maheshwari, 2018). PGPR as an important group of useful microorganisms in the rhizosphere can boost the availability of micro- and macronutrients in the growing environment of plants by different mechanisms (Glick, 2012; Etesami, 2018b; Etesami and Maheshwari, 2018). For example, IAA-producing PGPR improve nutrient and water uptake, which may have positive effects on plant growth as a whole, by altering root architecture and increasing total root surface area under nutrient-deficient conditions (Somers et al., 2008; Glick, 2012; Etesami et al., 2015a; Etesami and Alikhani, 2016). In general, by mobilizing micro- and macronutrients in the rhizosphere and by producing phytohormones (especially IAA), siderophore production (increment in availability of Fe, Zn, etc.), ACC deaminase activity (decreased stress ethylene and increased root elongation), and phosphate solubilization, PGPR can alleviate nutritional imbalance-induced stress in stressed plants (Etesami and Beattie, 2017; Etesami, 2018b; Etesami and Maheshwari, 2018). These beneficial rhizobacteria are involved in the geochemical cycling of micro- and macronutrients and determine their availability for soil microbial community and plants via different action mechanisms (Fig. 15.3). In this section, the ways in which PGPR can be applied to augment crop health and productivity in micro- and macronutrient poor environments are briefly discussed. The discussion focuses on the most important macronutrient (nitrogen, phosphorus, and potassium) and micronutrients that their deficiency has a significant effect on plant growth and yield in agricultural land. 15.5.1.1 Nitrogen Nitrogen (N) is an important element in plant growth and development and is a component of chlorophyll molecules and, therefore, plays an important role in photosynthesis (Mus et al., 2016). This nutrient is also considered as a limiting nutrient for both natural and agricultural ecosystems (Uchida, 2000; Etesami and Beattie, 2017). N is one of the most abundant elements in the Earth’s atmosphere (in the form of N2). But plants are not able to use this form of N and can only use reduced forms of this element. Only a specialized group of prokaryotes is able to convert N2 to ammonia (NH3) by enzyme nitrogenase. Plant-associated beneficial bacteria can augment plant N uptake by processes such as the symbiotic N2 fixation and nonsymbiotic N2 fixation (nitrogen fixation by associative and free-living bacteria) (Wagner, 2011; Santi et al., 2013), mineralizing organic forms of N (i.e., amino acids, peptides or proteins, and nucleic acids) in soil and converting them into absorbable forms of the plant, and augmenting root system of plants by production of

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FIGURE 15.3 Beneficial traits of PGPR toward nutritional imbalance stress tolerance in plants grown in nutrient-poor soils. Broken arrows show rhizobacterial components neutralizing nutritional imbalance stress effects. ACC-deaminase-producing PGPR decrease the excessive ethylene production in plants caused by nutritional imbalance stress and thereby eliminate the negative effect of ethylene on roots. Production of phytohormones increases the overall growth and also alters root characteristics (i.e., alteration of root proliferation, metabolism, and respiration rate) to facilitate uptake of nutrients. Phytohormone IAA also increases the size of aerial parts of the plants. Bacterial IAA can also loosen the cell walls of the plant, which increases the exudation of the root and provides additional nutrients to support the growth of the rhizosphere bacteria. The higher release of nutrients in turn increases the microbial activity and then IAA, and this process continues in a cycle. ACC deaminase producing PGPR can increase root growth and root length by decreasing stress ethylene and thereby increase plant growth and root exudates. Root exudates, due to having organic acids, proton, phytosiderophores, enzymes (e.g., xylanase, phosphatase, RNase, polygalacturonase, protease, sucrase, and urease), and chelating agents can also increase the amount of insoluble elements (such as P and micronutrient) in the rhizosphere. KSB decrease the pH by production of organic acids and protons. The transformation of fixed forms of K, that is, silicate minerals, by organic acids results in a significant increase in the level of available K in soil solution, which plants can uptake easily. KSB produce chelated compounds that make complexes with K and enhance its availability. KSB also increase K availability by acidolysis of the surrounding area of microorganism. This acidolysis by KSB via releasing organic acids breaks K mineral, resulting in slow liberation of readily bioavailable form of K in soil solution. Bacterial-mediated acidolysis can also promote the production of chelates of metals linked with K minerals. The bacteria help exudation of soluble compounds, decomposition of soil organic matter, and mobilization and mineralization of other nutrients (Ahmad et al., 2016). The colonization of plant by IAA and ACC deaminase producing bacteria makes capable the plants to explore more soil that might have improved the uptake of micro- and macronutrients indirectly. EPS serve as attachment structures to mineral or rock surface that can affect the mineral dissolution by forming complexes with framework ions in solution. KSB also synthesize biofilms, which create controllable microenvironments around microbial cells for weathering. Rhizospheric biomass of bacteria captures a significant amount of released nutrients (i.e., N, P, and K) that serves as a potential source of available nutrients for plants. ACC, 1-Aminocyclopropane-1-carboxylate; IAA, indole-3-acetic acid; KSB, potassium solubilizing bacteria; and PGPR, plant growth promoting rhizobacteria.

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IAA and ACC deaminase (the increase of the plant’s access to more volumes of soil and absorbing more N from the depths of the soil) (Diby et al., 2005b; Theunis, 2005; Paul and Sarma, 2006; Etesami et al., 2009, 2014a,b; Glick, 2012; Etesami and Alikhani, 2016; Etesami and Maheshwari, 2018). 15.5.1.2 Phosphorus Phosphorus (P) is an essential element for all living things. The presence of this element as a combination of any living cell is inevitable, because no other element can replace its vital role in many physiological and biochemical processes. Unlike nitrogen that the atmosphere is one of its major sources, this element does not have such a source (Ezawa et al., 2002). Unlike other macronutrients, this element has the least mobility in the soil and plant. On average, most mineral elements in the soil solution are present in mM amounts, while P is present in a μM amount (Ozanne, 1980). P is taken up in monobasic (H2PO42) or dibasic (HPO422) soluble forms (Syers et al., 2008). In general, P is present in two organic and inorganic forms in the soil and is in the range of 400 1200 mg/kg (Rodrı´guez and Fraga, 1999). Mineral P is found in the soil as calcium, aluminum, and iron compounds. Calcium phosphates predominate in neutral to alkaline soils, while in acidic soils, iron, and aluminum phosphates are dominant (Wakelin et al., 2004). Phytin, phospholipids, and nucleic acids are of organic forms of P. Phytic acid (known as inositol hexakisphosphate) is the most important P organic compound. Notwithstanding the abundance of both inorganic forms and organic P ones in soils (Richardson and Simpson, 2011), majority of P in soils is biologically unutilizable to plants. Most of this P is as adsorbed to soil mineral surfaces or as sparingly utilizable precipitates, associated with soil organic matter, and incorporated within microbial biomass (Etesami and Maheshwari, 2018). The concentration of soluble P in the soil is usually very low, and its content is 1 mg/kg or less (Paul, 2007). Very low levels of absorbable P in the rhizosphere cause this element to be recognized as one of the main limiting factors of plant growth in many ecosystems. Microorganisms, especially those that have the ability to dissolve insoluble phosphates, play a substantial role in all three major components of the soil P cycle. This cycle include mineralization, immobilization, dissolution, precipitation, sorption, and desorption (Sharma et al., 2013; Etesami and Maheshwari, 2018). Compared to fungi, bacteria are more effective at solubilizing phosphate and have a high population density (Alam et al., 2002). PSB and their interactions in soil intercede the distribution of P between the accessible P pool in soil solution and the total soil P by solubilizing and mineralizing insoluble phosphate compounds, immobilizing P into microbial biomass, and/or forming sparingly accessible forms of inorganic and organic soil P (Khan et al., 2007; Sharma et al., 2013). The ability of some bacteria to convert insoluble P into a usable form, such as orthophosphate, is an important feature of the PGPR that increase plant yield. Species from Pseudomonas, Bacillus, Enterobacter, Pantoea, and Rhizobium are the strongest phosphate solubilizers (Sharma et al., 2013). The main mechanisms for solubilizing mineral phosphate are the production of organic acids. In mineralizing organic P forms, acid phosphatases play a major role in the soil. Most of the soil microbial population is in the rhizosphere, and PSB differ in terms of type and population distribution in different soil conditions, and its population depends on the physical and chemical characteristics of the soil, the amount of organic matter and its phosphorus and agricultural operations. The relationship

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between plants and PSB is known as a synergistic or exacerbating relationship in nature. Because on the one hand, the PSB provide soluble P for the plant, and on the other hand, the plant releases the necessary carbon compounds (mainly sugars) through the root extracts to grow the PSB (Perez et al., 2007). The dissolution of mineral phosphates is related to the ability of microorganisms to release metabolites, such as the release of hydrogen ions and organic acids. It is known that organic and inorganic acids with their carboxylic and hydroxyl groups chelate the cations along with phosphate anion (Al31, Fe31, and Ca21), thereby also contributing to the dissolution of phosphate. Some researchers also believe that the dissolution of phosphate is the result of the anionic exchange of PO432 with organic acid anions (Omar, 1997). Universally, according to previous studies, many mechanisms have been reported, which by PSB can convert insoluble phosphates into absorbable P forms of the plant. Each PSB can function in one or more than one path to bring about the insoluble P solubilization (Sharma et al., 2013; Etesami and Maheshwari, 2018). Acidification (secretion of H1), chelation, release of complexing compounds or mineral-dissolving compounds (e.g., organic acid anions, protons, hydroxyl ions, CO2), exchange reactions, secretion of siderophores, IAA production, production of EPS, ACC deaminase activity, release of organic acids such as gluconic acid, lactic acid, acetic acid, isobutyric acid, glycolic acid, oxalic acid, glyoxylic acid, malonic acid, formic acid, and glycolic acid, and succinic acid (by decrease of pH and anion exchange or binding to Fe or Al) and inorganic acids such as nitric acid, carbonic acid, hydrochloric acid, and sulfuric acid, and mineralization of organic phosphates by secreting a variety of different extracellular phosphatases (acidic and alkaline phosphates convert organic phosphates, as a substrate, into mineral phosphates) have been reported as some of the mechanisms of dissolving insoluble phosphates by K-solubilizing bacteria (KSB) (Illmer and Schinner, 1995; Borch et al., 1999; Gyaneshwar et al., 2002; Stamford et al., 2003; Rashid et al., 2004; Hamdali et al., 2008; Yi et al., 2008; Sharma et al., 2013; Etesami et al., 2015a; Etesami and Maheshwari, 2018). 15.5.1.3 Potassium Potassium (K) is one of the essential macronutrients of plants, which plays a very important role in photosynthesis, cell division and growth, protein production, activity of enzymes, quantity and quality of products, and in the water economy for plants (Saber and Zanati, 1984; Etesami et al., 2017). Sufficient K in soil not only improves plant growth, but also increases plant tolerance under stress conditions, such as drought stress (Tisdale et al., 1985). Plants absorb K mainly in the form of K1 from soil solution. The amount of soluble K in soils is very variable and is typically between 1 and 10 mg/kg. Most of the soil K is not directly available for plant uptake (Zo¨rb et al., 2014), although there are large reserves of K in soils. In general, K deficiency is becoming one of the major constraints in crop production (Meena et al., 2014; Meena et al., 2016). Compared to the past, plants are recently responded well to K fertilization in soils. Reasons such as (1) intensive cropping; (2) imbalanced fertilizer application; (3) low application of K-fertilizers; (4) the presence of insoluble K sources; (5) introduction of high-yielding crop varieties and hybrids during green revolution; and (6) runoff, soil erosion, and K leaching have made the K availability low to plants (Zo¨rb et al., 2014).

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The most important sources of K in mineral soils are primary aluminosilicates, including feldspars and micas. K is also present in minerals such as vermiculite and illite (Sparks and Huang, 1985). Most soils have relatively high amounts of total K (mineral K, 90% 98% of total K, and nonexchangeable K, 1% 2% of total K), but their available K is relatively low. Among different forms of K, its soluble and exchangeable forms are usable to plant and the rest of the forms (mineral K and nonexchangeable K) are almost unusable to the plants. Therefore mineral K and nonexchangeable K forms should be converted into exchangeable K (1% 2% of total K) and solution K forms (Haby et al., 1990). Biochemical processes involved in the weathering of K-bearing minerals occur mainly in microbial environments and are affected by microorganisms (Etesami et al., 2017). Among these microorganisms, the role of KSB, as an important group of PGPR, is gaining importance in modern agriculture for augmenting K availability in soil and sustainable crop production. The use of KSB in agriculture has been known as one of the effective technologies to fulfill the K requirement of crop plants (Ahmad et al., 2016; Meena et al., 2016; Sindhu et al., 2016). By converting mineral K into available K (solution K), KSB (i.e., Bacillus mucilaginosus, Bacillus circulans, Bacillus edaphicus, Paenibacillus spp., Pseudomonas, Acidithiobacillus ferrooxidans, and Burkholderia) showed a significant role in providing K to plants (Parmar and Sindhu, 2013; Sindhu et al., 2016; Etesami et al., 2017). The effectiveness of the KSB in the solubility of K-bearing minerals and releasing K is influenced by many factors, including the size, amount, and type of soil K-bearing minerals, the type of microorganisms used in solubilizing these minerals, nutritional status of soil, and environmental factors (Sindhu et al., 2016). According to published studies, little information is now available on mechanisms used by KSB to solubilize K-bearing minerals and release soluble K (Etesami et al., 2017). Based on the findings of previous studies, the K solubilization mechanisms by PGPR is almost similar to P solubilization mechanisms. Some of the most important solubilization mechanisms for solubilizing K-containing minerals (i.e., mica, muscovite, and biotite feldspar) and releasing K by KSB, which have so far been known in previous studies, include release of H1 (H1 ions displace K1, Mg21, Ca21, and Mn21 from the cation-exchange complex in a soil), synthesis of organic acids such as oxalic acid, glycolic acid, tartaric acids, lactic acid, gluconic acid, citric acid, malic acid, 2-ketogluconic acid, succinic acid, propionic acid, fumaric acid, and malonic acid (decreasing soil pH and chelating Si41, Al31, Fe21, and Ca21 ions associated with K-bearing minerals) and inorganic acids, production of capsular polysaccharides, hydroxyl anion, extracellular polysaccharides (serving as attachment structures to mineral or rock surface and forming complexes with framework ions in solution), siderophores, formation of biofilms on the rhizospheric mineral surfaces (increasing the residence time of water as compared to the residence time at the bare rock or mineral surface and augmenting mineral weathering), storing K in their biomass (a significant quantity of fixed K), organic ligands, and extracellular enzymes (Uroz et al., 2009; Parmar, 2010; Huang et al., 2013; Meena et al., 2014; Ahmad et al., 2016; Etesami et al., 2017). Other PGPR such as siderophore, IAA and ACC deaminase producing bacteria, and PSB can indirectly augment the availability of K for the plant by enhancing the plant root system (increase in plant access to more volumes of soil and nutrients present in it) and the exudates of the root (the presence of chelating agents, pH-decreasing compound, and nutrients and carbon compounds to increase the further activity of PGPR in root

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exudates) and solubilization of insoluble nutrients such as P and Fe (Etesami et al., 2015b, 2017; Etesami and Maheshwari, 2018). 15.5.1.4 Microelements (trace minerals) Elements such as iron (Fe), manganese (Mn), zinc (Zn), copper (Cu), boron (B), molybdenum (Mo), and chlorine (Cl), in some sources, nickel (Ni) and cobalt (Co), are considered as micronutrients. As with macronutrients, the presence of micronutrients in an available form is also essential for the growth of plants. Micronutrients have a special place in agricultural production, despite their low requirements (Welch and Shuman, 1995). The concentration of most of these elements in the soil is pH-dependent, and their concentration in alkaline pH is very low. For example, in calcareous soils, in comparison with acid soils, the lack of these elements is more significant. Organic matter plays an essential role in the cycle of micronutrients. The materials as natural chelating agents are bonded with micronutrients in the soil and move them toward the plant roots. Also, organic matter can modify the pH of the environment around the root and thereby help absorb micronutrients by the plant roots. Bioavailability of the micronutrients is also limited due to the low mobility and partial availability of these elements in the soil. It is well known that plant-associated beneficial rhizobacteria can augment the availability of these elements to plants by mechanisms such as diminishing rhizosphere soil pH and producing chelating agents (Miransari, 2013; Etesami et al., 2015a; Etesami and Maheshwari, 2018). For example, IAA and ACC deaminase producing bacteria can increase the plant’s access to these elements with low mobility from different soil depths by increasing the root system of the plant (Etesami et al., 2015a). Many IAA- and siderophore-producing rhizobacteria strains could augment Fe nutrition (Jin et al., 2006; Ramos-Solano et al., 2010; Etesami et al., 2015a; Etesami and Maheshwari, 2018). Most plant-associated rhizobacteria generate iron chelators, which are called siderophores (low molecular weight organic compounds), in response to low iron levels in the root environment. In addition to having high affinity to bind Fe31 and increasing its availability, siderophores can also augment the availability of other metal ions (Boukhalfa and Crumbliss, 2002; Ramos-Solano et al., 2010; Etesami, 2018a). According to Latour et al. (2009), the ligand exchange is another theory on the supply of Fe(III) by siderophores. Due to higher affinity of phytosiderophores to Fe31 than bacterial siderophores, Fe supplied by bacterial siderophores interacts with phytosiderophores in a ligand exchange reaction and is finally taken up by the plant (Etesami and Beattie, 2017). The increment in availability of Mn to plants by some rhizobacteria (i.e., Bacillus, Pseudomonas, and Geobacter) has also been reported. These PGPR could reduce oxidized Mn41 (a plant-unavailable Mn form) to Mn21 (a plant-available Mn form) (Osorio Vega, 2007; Etesami and Maheshwari, 2018). IAA- and ACC deamiunase producing rhizobacteria augment Mn availability in plant growth environment under the stress of deficiency of the element by the increment of the root system of the plant and thereby increasing the exudates of the root (Dutta and Podile, 2010; Miransari, 2011; Etesami and Beattie, 2017; Etesami and Maheshwari, 2018). The electrons and protons required for the reduction of MnO2 to Mn21 are achieved through the decomposition of carbonaceous compounds present in bacterial activities mediated root exudates and proton excretion system of root cells (PGPR-induced increase of root system), respectively (Etesami et al., 2015a; Etesami and Maheshwari, 2018). PGPR can also prevent the reprecipitation of Mn, Fe, and

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other microelements through the secretion of chelating agents such as phenolic compounds and organic acids that form soluble complex with these micronutrients (Etesami, 2018b; Etesami and Maheshwari, 2018). PGPR can, through various mechanisms, boost the availability of Cu and Zn for plants under conditions of deficiency of these micronutrients. For example, these bacteria can increase the availability of Cu and Zn in plant growth medium (rhizosphere) through the production of various metabolites, such as siderophore (formation of Zn/Cu-siderophore complex), organic acids (reduced rhizosphere pH), and other chelating agents (e.g., carboxylates and phenolic compounds). On the other hand, through the production of IAA, these bacteria can lead to increased plant root exudates (Etesami et al., 2015a). These secretions also contain phytosiderophores, organic acids, and other metal-chelating agents that can in turn augment the availability of these micronutrients to micronutrient-stressed plants (Badri and Vivanco, 2009; Iqbal et al., 2010; Etesami and Maheshwari, 2018). In addition to augmenting the availability of the micronutrients under conditions of deficiency of these elements, the PGPR can also alleviate high micronutrient concentrations mediated unfavorable effects on plant growth and environment by various mechanisms (Zhuang et al., 2007; Etesami and Maheshwari, 2018). As an example, under flooded conditions, the accumulation of iron leads to bronzing symptoms in leaves of plants. Under such conditions (anaerobic conditions), ferric oxide hydrate complexes are reduced, and the Fe(II) is released from these compounds, which can even be toxic for the rice roots (Doberman and Fairhurst, 2000). By enhancing the Fe availability locally, decreasing Fe(II) toxicity to the plant and accumulating the complexed metal into the bacterial cells, siderophores-producing PGPR may capture iron(III), produced by oxidation of Fe(II) in oxic microniches into the plant or in the environment around the plant’s roots (rhizosphere) (Loaces et al., 2011). In addition, it has been proven that siderophore-producing PGPR can also be beneficial to the plants that are subjected to heavy metal induced stress. Under such conditions (increased the availability of heavy metals in the plant growth medium), siderophoreproducing bacteria can augment the availability of iron considerably (the high affinity of bacterial siderophores to iron in comparison to other metals) (Etesami and Maheshwari, 2018). Since influx carriers of some of the heavy metals to plants are similar to that of the iron to plants, the iron can be further absorbed by heavy metal stressed plant, due to high concentrations, compared with other heavy metals, which in turn alleviate the heavy metal induced stress (Braud et al., 2006; Glick, 2012; Etesami, 2018a).

15.6 Conclusions and future prospects Abiotic stresses are one of the most important threats to plants. Development of stresstolerant cultivars through plant breeding or genetic engineering is one of the strategies to combat nonliving tensions, but it is a long and time-consuming process. While the use of beneficial microorganisms associated with plants to reduce these stresses is an affordable and environmentally friendly strategy, the possibility of reducing nonbiological stress mediated damage by using useful microorganisms opens a new window in agriculture and can be considered as an important step toward achieving a sustainable

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agricultural system and organic production. The most important point is that PGP microorganisms can induce endurance in plants against a variety of abiotic and biotic stresses, so the isolation, screening, and application of these microorganisms can be very valuable. Since the microorganisms isolated from stressed habitats are more efficient to augment the plant endurance to abiotic stresses than those isolated from nonstressed habitats, the microorganisms isolated from the rhizosphere of plants grown in stressed environments can be used to augment the growth and possibly the yield of crop plants and to engender sustainable agriculture in stress-affected areas. The PGPR, as an alternative approach for alleviating abiotic stresses, are a viable and sustainable alternative to get better stressaffected agricultural areas, without application of chemical fertilizers that contaminate water and agricultural soils. These PGPR may be able to augment soil quality, soil microbial communities, and agriculture yield of crop plants in arid and semiarid environments (the harsh salinity and drought conditions) and can be exploited in biofertilizer formulates to sustain crop production in saline soil-based agriculture. Established upon the knowledge produced until now, multifold future routes of research approaches are suggested to do in the future studies: 1. Albeit some lucrative effects of microorganisms on stressed plants have been well known, ranging from the secretion of bioactive compounds to interposition in plant hormonal signaling, many of the underlying physiological and molecular mechanisms are still essential to be identified to make optimal the agronomic uses of these microorganisms in stress agriculture. Understanding these mechanisms and completing the mechanisms expressed by any microbial inoculum are important in advancing research on growth potentials and protective effects of plants in this area. In addition, the number of traits needed to effectively protect plants from environmental stresses has remained elusive. 2. While some research are pertinent to the structure of bacterial associates in plants and their potentially beneficial effects, very little has been known about the mechanisms by which the bacterial and fungal microbiome associated with stressed plants could enhance plant resistance to extreme stress as well as how their effect on phenotype of stressed plants. 3. Since the diversity of PGPRs in stressed soils and in the microbiome of stressed plants relies on soil parameters and the plant species, further research on diversity of the microbial community in the rhizo- and endosphere of various plants in different areas is needed to illuminate and characterize this ecological association in stress agriculture. 4. At the present time, there is little information about the signaling mechanisms and establishment interactions between PGPR and plants, especially in field applications. Therefore it is necessary to extend and enhance the studies of plant PGPR interactions, their adaptation in stressed environment and the ecology of these bacteria in natural lodgings. 5. More knowledge about characterizations of the PGPR associated with stressed plants, the mechanisms of their survival and protection against abiotic stresses, and their interaction with plants is essential to develop strategies for plant protection in stress agriculture.

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6. The inefficiency of PGPR in field conditions or natural conditions is one of the most common problems with the use of these microbial inoculants. This inefficiency is mainly due to the fact that the bacteria have been isolated from an environment different from the environment (such as variations in soil type, management practices, and climate) in which the plant grows. Therefore it is necessary to isolate PGPR with high efficiency from various rhizosphere environments under different conditions (e.g., alkaline, acids, salinity, drought, high and low temperatures, and flooded), so that they can withstand environment alterations that crops are exposed today (Etesami and Beattie, 2018). 7. The biological characteristics and factors influencing the PGP ability of stress tolerantPGPR need to be studied further. In addition, further optimization is required for application of the stress-tolerant PGPR isolated from stressed plants to introduce to nonstressed crops in stress agriculture. 8. A greater understanding of the molecular mechanisms by which stress-tolerant PGPR boost plant resistance to abiotic stresses will allow us to increase the ability of these bacteria to stimulate plant growth and augment plant tolerance to abiotic stresses via genetic engineering. In addition, inserting the stress-resistant genes of these bacteria to plants may facilitate and improve interactions the plants with PGPR. 9. In addition to studying the endophytic and rhizospheric bacteria associated with various plants, isolating and identifying endophytic and rhizospheric fungi and analyzing their interaction with host plants will help the survival of both partners under stress conditions. Knowing about the interactions (i.e., the mechanisms that govern the specificity of the interaction between fungi and stressed plants, and characterization of plant growth promoting traits of the fungi isolated from stressed plants) between these microorganisms and stressed plants will be essential to develop strategies for protecting stressed plants and nonstressed plants. Usually, endophytic microorganisms may be of particular importance because these microorganisms do not need to compete for nutrients with other autochthonous microorganisms. Moreover, these microorganisms are protected from severe environmental stresses (higher efficiency of endophytic microorganisms in alleviating the adverse effects of stresses on plants compared to rhizosphere microorganisms) (Etesami and Maheshwari, 2018). In addition to satisfying augmented need of food production in the frame of a boosting world population and ongoing climate changes, the examination of the rhizobacterial community associated with stressed plants might result in multifold knowledge outputs including (1) the comprehension of the interaction between plant and PGPR under stress conditions, for example, finding the mechanisms that govern the specificity of the interaction between PGPR and stressed plants, studying the composition of root exudates and their effect on the mediation of plant PGPR interactions in the rhizosphere (their effect on bacterial colonization) and on regulation of the expression of genes related to plant growth improvement and biocontrol in PGPR, and also studying bacterial volatiles and secretions (bacterial metabolites, i.e., IAA, siderophores, EPS) and their effect on increased plant root exudation; (2) the comprehension of the mechanisms underlying improvement of plant growth under stress (identification of the exudates, signals, key players in the rhizosphere microbiome, and other characterizations of plant growth promoting traits of PGPR under

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stress); (3) the understanding of the genetic and biochemical basis of symbiotic relationships responsible for stress endurance; and (4) identification of PGPR to design bacterial inoculants exploitable for agriculture in arid and saline lands (Etesami and Maheshwari, 2018). In general, the victorious utilization of PGPR in different applications (i.e., phytoremediation, phytodesalinization, biofertilization, and biocontrol) relies on their ability to be established in the presence of types of autochthonous microorganisms and abiotic and biotic stresses in the applied area. It has been reported that PGPR effective at augmented plant growth and resistance to biological and abiotic stresses in greenhouse and in vitro conditions could not do this in field conditions, which was often due to inadequate colonization of rhizo- and endosphere of inoculated plants (Compant et al., 2010). Many variables, including physical, chemical, and biological attributes of the soil, natural selection, and agricultural management proceedings such as application of chemical and organic fertilizers and pesticides and rotation of crop have been known to affect the ability of preselected PGPR to colonize the inoculated plant. To prevail over the inconsistencies, one way is to coinoculate plants with the PGPR strains (the application of stress tolerant microbial consortium of bacterial strains and fungi) with multiple PGP properties (Etesami and Maheshwari, 2018). Since PGPR have multiple beneficial effects, which can be complemented by miscellaneous phenomena, the simultaneous use of several bacteria instead of a bacterium has an increasing effect (a synergistic effect) on alleviating different stresses. The combined use of PGPR with stress-tolerant beneficial fungi (especially arbuscular MF) in agricultural may be a suitable and promising approach in stressful agricultural environments (Ghorchiani et al., 2018). In most of the past studies the efficacy of PGPR has been evaluated in the presence of an environmental stress. However, since we now face a series of environmental stresses, it is better to check the effectiveness of these bacteria (PGPR), in order to select the most effective bacteria, in the presence of several stresses, such as drought, heavy metals, salinity, and imbalance of micro- and macronutrients, simultaneously (Etesami and Maheshwari, 2018). It has been well established that PGPR can stimulate plant growth under controlled and greenhouse conditions. Based on the results of these (in vitro and greenhouse) studies, many bacteria have been introduced as plant growth promoter (biofertilizer). However, some of these bacteria could not increase plant growth under field conditions as well because soil conditions such as sorption capacity of nutrients, acid and alkaline pH, soil nutrients status, environmental (abiotic and biotic) stresses, and native microorganisms affect the survival and plant growth promoting activities of the introduced PGPR under natural or field conditions. But the main goal of doing this early study is to achieve PGPR that could increase plant growth under natural conditions. Therefore in order to achieve the most effective PGPR and introduce them as biofertilizer, it is needed to study plant growth promoting potential of the PGPR (the bacteria that were positive in terms of promoting plant growth under in vitro and greenhouse conditions) under field conditions, on a large scale, and in the long run.

Acknowledgment I wish to thank University of Tehran for providing the necessary facilities for this study.

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References Abbas, T., Balal, R.M., Shahid, M.A., Pervez, M.A., Ayyub, C.M., Aqueel, M.A., et al., 2015. Silicon-induced alleviation of NaCl toxicity in okra (Abelmoschus esculentus) is associated with enhanced photosynthesis, osmoprotectants and antioxidant metabolism. Acta Physiol. Plant. 37, 1 15. Acosta-Martı´nez, V., Dowd, S., Sun, Y., Allen, V., 2008. Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol. Biochem. 40, 2762 2770. Adrees, M., Ali, S., Rizwan, M., Zia-ur-Rehman, M., Ibrahim, M., Abbas, F., et al., 2015. Mechanisms of siliconmediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol. Environ. Saf. 119, 186 197. Ahemad, M., 2012. Implications of bacterial resistance against heavy metals in bioremediation: a review. J. Inst. Integr. Omics Appl. Biotechnol. (JIIOAB) 3, 39 46. Ahemad, M., 2014. Remediation of metalliferous soils through the heavy metal resistant plant growth promoting bacteria: paradigms and prospects. Arab. J. Chem. 1 13. Ahemad, M., Kibret, M., 2013. Recent trends in microbial biosorption of heavy metals: a review. Biochem. Mol. Biol. 1, 19 26. Ahmad, M., Nadeem, S.M., Naveed, M., Zahir, Z.A., 2016. Potassium-solubilizing bacteria and their application in agriculture. In: Meena, V.S., Maurya, B.R., Verma, J.P., Meena, R.S. (Eds.), Potassium Solubilizing Microorganisms for Sustainable Agriculture. Springer, New Delhi, pp. 293 313. Alam, S., Khalil, S., Ayub, N., Rashid, M., 2002. In vitro solubilization of inorganic phosphate by phosphate solubilizing microorganisms (PSM) from maize rhizosphere. Int. J. Agric. Biol. 4, 454 458. Alami, Y., Achouak, W., Marol, C., Heulin, T., 2000. Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. Strain isolated from sunflower roots. Appl. Environ. Microbiol. 66, 3393 3398. Ali, S., Charles, T.C., Glick, B.R., 2014. Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol. Biochem. 80, 160 167. Ali, S., Chaudhary, A., Rizwan, M., Anwar, H.T., Adrees, M., Farid, M., et al., 2015. Alleviation of chromium toxicity by glycine betaine is related to elevated antioxidant enzymes and suppressed chromium uptake and oxidative stress in wheat (Triticum aestivum L.). Environ. Sci. Pollut. Res. 22, 10669 10678. Amellal, N., Burtin, G., Bartoli, F., Heulin, T., 1998. Colonization of wheat rhizosphere by EPS-producing Pantoea agglomerans and its effects on soil aggregation. Appl. Environ. Microbiol. 64, 3740 3747. del Amor, F.M., Cuadra-Crespo, P., 2012. Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper. Funct. Plant Biol. 39, 82 90. Anjum, S., Wang, L., Farooq, M., Xue, L., Ali, S., 2011. Fulvic acid application improves the maize performance under well-watered and drought conditions. J. Agron. Crop Sci. 197, 409 417. Archana, G., Buch, A., Kumar, G.N., 2012. Pivotal role of organic acid secretion by rhizobacteria in plant growth promotion. Microorganisms in Sustainable Agriculture and Biotechnology. Springer, pp. 35 53. Arkhipova, T.N., Prinsen, E., Veselov, S.U., Martinenko, E.V., Melentiev, A.I., Kudoyarova, G.R., 2007. Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292, 305 315. Armada, E., Rolda´n, A., Azcon, R., 2014. Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and Salvia plants species under drought conditions in natural arid soil. Microb. Ecol. 67, 410 420. Arora, N.K., Singhal, V., Maheshwari, D.K., 2006. Salinity-induced accumulation of poly-β-hydroxybutyrate in rhizobia indicating its role in cell protection. World J. Microbiol. Biotechnol. 22, 603 606. Ashraf, M., Ahmad, A., McNeilly, T., 2001. Growth and photosynthetic characteristics in pearl millet under water stress and different potassium supply. Photosynthetica 39, 389 394. Ashraf, M., Hasnain, S., Berge, O., Mahmood, T., 2004. Inoculating wheat seedlings with exopolysaccharideproducing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol. Fertil. Soils 40, 157 162. Awad, N., Turky, A., Abdelhamid, M.T., Attia, M., 2012. Ameliorate of environmental salt stress on the growth of Zea mays L. plants by exopolysaccharides producing bacteria. J. Appl. Sci. Res. 8, 2033 2044. Badri, D.V., Vivanco, J.M., 2009. Regulation and function of root exudates. Plant Cell Environ. 32, 666 681. Bailly, A., Weisskopf, L., 2012. The modulating effect of bacterial volatiles on plant growth: current knowledge and future challenges. Plant Signaling Behav. 7, 79 85.

Plant Life under Changing Environment

References

385

Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., Vivanco, J.M., 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233 266. Bal, H.B., Nayak, L., Das, S., Adhya, T.K., 2013. Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil 366, 93 105. Baligar, V.C., Fageria, N.K., He, Z.L., 2001. Nutrient use efficiency in plants. Commun. Soil Sci. Plant Anal. 32, 921 950. Baluˇska, F., 2013. Inhibition of Root Growth by Salinity Stress: Toxicity or an Adaptive Biophysical Response? Springer Science & Business Media, p. 299. Banaei-Asl, F., Bandehagh, A., Uliaei, E.D., Farajzadeh, D., Sakata, K., Mustafa, G., et al., 2015. Proteomic analysis of canola root inoculated with bacteria under salt stress. J. Proteomics 124, 88 111. Barcelo´, J., Poschenrieder, C., 1990. Plant water relations as affected by heavy metal stress: a review. J. Plant Nutr. 13, 1 37. Barnawal, D., Bharti, N., Pandey, S.S., Pandey, A., Chanotiya, C.S., Kalra, A., 2017. Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol. Plant. 161, 502 514. Beattie, G.A., 2007. Plant-associated bacteria: survey, molecular phylogeny, genomics and recent advances. PlantAssociated Bacteria. Springer, pp. 1 56. Belimov, A.A., Dodd, I.C., Hontzeas, N., Theobald, J.C., Safronova, V.I., Davies, W.J., 2009. Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol. 181, 413 423. Berendsen, R.L., Pieterse, C.M.J., Bakker, P.A.H.M., 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478 486. Berg, G., Smalla, K., 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1 13. Bharti, N., Barnawal, D., Awasthi, A., Yadav, A., Kalra, A., 2014. Plant growth promoting rhizobacteria alleviate salinity induced negative effects on growth, oil content and physiological status in Mentha arvensis. Acta Physiol. Plant. 36, 45 60. Bharti, N., Pandey, S.S., Barnawal, D., Patel, V.K., Kalra, A., 2016. Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci. Rep. 6, 34768. Bhattacharyya, P.N., Jha, D.K., 2012. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J. Microbiol. Biotechnol. 28, 1327 1350. Bibi, S., Husain, S.Z., Malik, R.N., 2008. Pollen analysis and heavy metals detection in honey samples from seven selected countries. Pak. J. Bot. 40, 507 516. Bishop, P.L., Bishop, P.L., 2000. Pollution Prevention: Fundamentals and Practice. Waveland Press, 699 p. Bodner, G., Nakhforoosh, A., Kaul, H.-P., 2015. Management of crop water under drought: a review. Agron. Sustain. Dev. 35, 401 442. Borch, K., Bouma, T.J., Lynch, J.P., Brown, K.M., 1999. Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ. 22, 425 431. Botella, M., Martinez, V., Pardines, J., Cerda, A., 1997. Salinity induced potassium deficiency in maize plants. J. Plant Physiol. 150, 200 205. Boukhalfa, H., Crumbliss, A.L., 2002. Chemical aspects of siderophore mediated iron transport. Biometals 15, 325 339. Braud, A., Je´ze´quel, K., Vieille, E., Tritter, A., Lebeau, T., 2006. Changes in extractability of Cr and Pb in a polycontaminated soil after bioaugmentation with microbial producers of biosurfactants, organic acids and siderophores. Water Air Soil Pollut.: Focus 6, 261 279. Cao, X., Ma, L.Q., Singh, S.P., Zhou, Q., 2008. Phosphate-induced lead immobilization from different lead minerals in soils under varying pH conditions. Environ. Pollut. 152, 184 192. Casanovas, E.M., Barassi, C.A., Andrade, F.H., Sueldo, R.J., 2003. Azospirillum-inoculated maize plant responses to irrigation restraints imposed during flowering. Cereal Res. Commun. 395 402. Chakraborty, N., Ghosh, R., Ghosh, S., Narula, K., Tayal, R., Datta, A., et al., 2013. Reduction of oxalate levels in tomato fruit and consequent metabolic remodeling following overexpression of a fungal oxalate decarboxylase. Plant Physiol. 162, 364 378.

Plant Life under Changing Environment

386

15. Plant microbe interactions in plants and stress tolerance

Chakraborty, U., Chakraborty, B., Dey, P., Chakraborty, A.P., 2015. 15 Role of microorganisms in alleviation of abiotic stresses for sustainable agriculture. Abiotic Stresses in Crop Plants. CABI, Wallingford, pp. 232 253. Chatterjee, S., Sau, G.B., Mukherjee, S.K., 2009. Plant growth promotion by a hexavalent chromium reducing bacterial strain, Cellulosimicrobium cellulans KUCr3. World J. Microbiol. Biotechnol. 25, 1829 1836. Chen, M., Wei, H., Cao, J., Liu, R., Wang, Y., Zheng, C., 2007. Expression of Bacillus subtilis proBA genes and reduction of feedback inhibition of proline synthesis increases proline production and confers osmotolerance in transgenic Arabidopsis. BMB Rep. 40, 396 403. Chen, T.H.H., Murata, N., 2008. Glycine betaine: an effective protectant against abiotic stress in plants. Trends Plant Sci. 13, 499 505. ´ Chmielowska-Ba˛k, J., Gzyl, J., Rucinska-Sobkowiak, R., Arasimowicz-Jelonek, M., Deckert, J., 2014. The new insights into cadmium sensing. Front. Plant Sci. 5, 245. Cohen, A.C., Travaglia, C.N., Bottini, R., Piccoli, P.N., 2009. Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87, 455 462. Cohen, A.C., Bottini, R., Pontin, M., Berli, F.J., Moreno, D., Boccanlandro, H., et al., 2015. Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol. Plant. 153, 79 90. Compant, S., Cle´ment, C., Sessitsch, A., 2010. Plant growth-promoting bacteria in the rhizo-and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42, 669 678. Damodaran, T., Rai, R.B., Jha, S.K., Kannan, R., Pandey, B.K., Sah, V., et al., 2014. Rhizosphere and endophytic bacteria for induction of salt tolerance in gladiolus grown in sodic soils. J. Plant Interact. 9, 577 584. Diby, P., Sarma, Y.R., Srinivasan, V., Anandaraj, M., 2005b. Pseudomonas fluorescens mediated vigour in black pepper (Piper nigrum L.) under green house cultivation. Ann. Microbiol. 55, 171 174. Dimkpa, C., Weinand, T., Asch, F., 2009a. Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 32, 1682 1694. Dimkpa, C.O., Merten, D., Svatoˇs, A., Bu¨chel, G., Kothe, E., 2009b. Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol. Biochem. 41, 154 162. Doberman, A., Fairhurst, T., 2000. Rice: Nutrient Disorders and Nutrient Management. International Rice Research Institute (IRRI), Singapore, MY. Dutta, S., Khurana, S.M.P., 2015. Plant growth-promoting rhizobacteria for alleviating abiotic stresses in medicinal plants. Plant-Growth-Promoting Rhizobacteria (PGPR) and Medicinal Plants. Springer, pp. 167 200. Dutta, S., Podile, A.R., 2010. Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit. Rev. Microbiol. 36, 232 244. Egamberdieva, D., 2009. Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol. Plant. 31, 861 864. Egamberdieva, D., 2012. Pseudomonas chlororaphis: a salt-tolerant bacterial inoculant for plant growth stimulation under saline soil conditions. Acta Physiol. Plant. 34, 751 756. Egamberdieva, D., Kucharova, Z., 2009. Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol. Fertil. Soils 45, 563 571. Egamberdieva, D., Lugtenberg, B., 2014. Use of plant growth-promoting rhizobacteria to alleviate salinity stress in plants, Use of Microbes for the Alleviation of Soil Stresses, vol. 1. Springer, pp. 73 96. Endris, S., Mohammad, M.J., 2007. Nutrient acquisition and yield response of Barley exposed to salt stress under different levels of potassium nutrition. Int. J. Environ. Sci. Technol. 4, 323 330. Etesami, H., 2018a. Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicol. Environ. Saf. 147, 175 191. Etesami, H., 2018b. Can interaction between silicon and plant growth promoting rhizobacteria benefit in alleviating abiotic and biotic stresses in crop plants? Agric. Ecosyst. Environ. 253, 98 112. Etesami, H., Alikhani, H.A., 2016. Co-inoculation with endophytic and rhizosphere bacteria allows reduced application rates of N-fertilizer for rice plant. Rhizosphere 2, 5 12. Etesami, H., Beattie, G.A., 2017. Plant-microbe interactions in adaptation of agricultural crops to abiotic stress conditions. Probiotics and Plant Health. Springer, pp. 163 200. Etesami, H., Beattie, G.A., 2018. Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front. Microbiol. 9, 148.

Plant Life under Changing Environment

References

387

Etesami, H., Maheshwari, D.K., 2018. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol. Environ. Saf. 156, 225 246. Etesami, H., Alikhani, H.A., Jadidi, M., Aliakbari, A., 2009. Effect of superior IAA producing rhizobia on N, P, K uptake by wheat grown under greenhouse condition. World Appl. Sci. J. 6, 1629 1633. Etesami, H., Hosseini, H.M., Alikhani, H.A., Mohammadi, L., 2014a. Bacterial biosynthesis of 1aminocyclopropane-1-carboxylate (ACC) deaminase and indole-3-acetic acid (IAA) as endophytic preferential selection traits by rice plant seedlings. J. Plant Growth Regul. 33, 654 670. Etesami, H., Mirseyed Hosseini, H., Alikhani, H.A., 2014b. Bacterial biosynthesis of 1-aminocyclopropane-1caboxylate (ACC) deaminase, a useful trait to elongation and endophytic colonization of the roots of rice under constant flooded conditions. Physiol. Mol. Biol. Plants 20, 425 434. Etesami, H., Alikhani, H., Mirseyed Hosseini, H., 2015a. Indole-3-acetic acid and 1-aminocyclopropane-1carboxylate deaminase: bacterial traits required in rhizosphere, rhizoplane and/or endophytic competence by beneficial bacteria. In: Maheshwari, D.K. (Ed.), Bacterial Metabolites in Sustainable Agroecosystem. Springer International Publishing, pp. 183 258. Etesami, H., Alikhani, H.A., Hosseini, H.M., 2015b. Indole-3-acetic acid (IAA) production trait, a useful screening to select endophytic and rhizosphere competent bacteria for rice growth promoting agents. MethodsX 2, 72 78. Etesami, H., Emami, S., Alikhani, H.A., 2017. Potassium solubilizing bacteria (KSB): Mechanisms, promotion of plant growth, and future prospects—a review. J. Soil Sci. Plant Nutr. 17, 897 911. Evelin, H., Kapoor, R., Giri, B., 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann. Bot. 104, 1263 1280. Ezawa, T., Smith, S.E., Smith, F.A., 2002. P metabolism and transport in AM fungi. Plant Soil 244, 221 230. Feigin, A., 1985. Fertilization management of crops irrigated with saline water. Biosalinity in Action: Bioproduction with Saline Water. Springer, pp. 285 299. Franche, C., Lindstro¨m, K., Elmerich, C., 2008. Nitrogen-fixing bacteria associated with leguminous and nonleguminous plants. Plant Soil 321, 35 59. Gadd, G.M., 2010. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156, 609 643. Gaiero, J.R., McCall, C.A., Thompson, K.A., Day, N.J., Best, A.S., Dunfield, K.E., 2013. Inside the root microbiome: bacterial root endophytes and plant growth promotion. American Journal of Botany 100, 1738 1750. Geddie, J.L., Sutherland, I., 1993. Uptake of metals by bacterial polysaccharides. J. Appl. Bacteriol. 74, 467 472. Ghorchiani, M., Etesami, H., Alikhani, H.A., 2018. Improvement of growth and yield of maize under water stress by co-inoculating an arbuscular mycorrhizal fungus and a plant growth promoting rhizobacterium together with phosphate fertilizers. Agric. Ecosyst. Environ. 258, 59 70. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909 930. Glick, B.R., 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012, 963401. Glick, B.R., 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169, 30 39. Glick, B.R., 2015. Introduction to plant growth-promoting bacteria. In: Glick, R.B. (Ed.), Beneficial Plant-Bacterial Interactions. Springer International Publishing, Cham, pp. 1 28. ˆ .M., 2012. Anatomical characteristics and nutrient uptake and Gomes, M.P., Marques, T., Carneiro, M., Soares, A distribution associated with the Cd-phytoremediation capacity of Eucalyptus camaldulensis Dehnh. J. Soil Sci. Plant Nutr. 12, 481 496. Gond, S.K., Torres, M.S., Bergen, M.S., Helsel, Z., White, J.F., 2015. Induction of salt tolerance and up-regulation of aquaporin genes in tropical corn by rhizobacterium Pantoea agglomerans. Lett. Appl. Microbiol. 60, 392 399. Gray, E.J., Smith, D.L., 2005. Intracellular and extracellular PGPR: commonalities and distinctions in the plantbacterium signaling processes. Soil Biol. Biochem. 37, 395 412. Grieve, C.M., Grattan, S.R., 1999. Mineral nutrient acquisition and response by plants grown in saline environments, Handbook of Plant and Crop Stress, second ed. CRC Press, pp. 203 229. Grover, M., Ali, S.Z., Sandhya, V., Rasul, A., Venkateswarlu, B., 2011. Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J. Microbiol. Biotechnol. 27, 1231 1240.

Plant Life under Changing Environment

388

15. Plant microbe interactions in plants and stress tolerance

Gundala, P.B., Chinthala, P., Sreenivasulu, B., 2013. A new facultative alkaliphilic, potassium solubilizing, Bacillus sp. SVUNM9 isolated from mica cores of Nellore District, Andhra Pradesh, India. Research and reviews. J. Microbiol. Biotechnol. 2, 1 7. Guo, J., Chi, J., 2014. Effect of Cd-tolerant plant growth-promoting rhizobium on plant growth and Cd uptake by Lolium multiflorum Lam. and Glycine max (L.) Merr. in Cd-contaminated soil. Plant Soil 375, 205 214. Gupta, B., Huang, B., 2014. Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int. J. Genomics 2014, 1 18. Gyaneshwar, P., Kumar, G.N., Parekh, L.J., Poole, P.S., 2002. Role of soil microorganisms in improving P nutrition of plants. Food Security in Nutrient-Stressed Environments: Exploiting Plants’ Genetic Capabilities. Springer, pp. 133 143. Habib, S.H., Kausar, H., Saud, H.M., 2016. Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes, BioMed Res. Int., 2016. p. 6284547. Haby, V.A., Russelle, M.P., Skogley, E.O., 1990. Testing soils for potassium, calcium, and magnesium, (3rd ed.) SSSA, Madison, WI, pp. 181 227. Hamdali, H., Hafidi, M., Virolle, M.J., Ouhdouch, Y., 2008. Rock phosphate-solubilizing Actinomycetes: screening for plant growth-promoting activities. World J. Microbiol. Biotechnol. 24, 2565 2575. Hamdia, M.A.E.-S., Shaddad, M., Doaa, M.M., 2004. Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul. 44, 165 174. Hameed, A., Wu, Q.-S., Abd-Allah, E.F., Hashem, A., Kumar, A., Lone, H.A., et al., 2014. Role of AM fungi in alleviating drought stress in plants. Use of Microbes for the Alleviation of Soil Stresses. Springer, pp. 55 75. Hardoim, P.R., van Overbeek, L.S., Elsas, J.Dv, 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 16, 463 471. Hartmann, A., Schmid, M., Tuinen, Dv, Berg, G., 2008. Plant-driven selection of microbes. Plant Soil 321, 235 257. Hayat, R., Ali, S., Amara, U., Khalid, R., Ahmed, I., 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Ann. Microbiol. 60, 579 598. He, H., Ye, Z., Yang, D., Yan, J., Xiao, L., Zhong, T., et al., 2013. Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 90, 1960 1965. Heffernan, O., 2013. The dry facts. Nature 501, S2 S3. Heidari, M., Jamshid, P., 2010. Interaction between salinity and potassium on grain yield, carbohydrate content and nutrient uptake in pearl millet ARPN. J. Agric. Biol. Sci. 5, 39 46. Hichem, H., El Naceur, A., Mounir, D., 2009. Effects of salt stress on photosynthesis, PSII photochemistry and thermal energy dissipation in leaves of two corn (Zea mays L.) varieties. Photosynthetica 47, 517 526. Huang, Z., He, L., Sheng, X., He, Z., 2013. Weathering of potash feldspar by Bacillus sp. L11. Wei sheng wu xue bao 5 Acta Microbiol. Sin. 53, 1172 1178. Ilangumaran, G., Smith, D.L., 2017. Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front. Plant Sci. 8, 1768. Illmer, P., Schinner, F., 1995. Solubilization of inorganic calcium phosphates—solubilization mechanisms. Soil Biol. Biochem. 27, 257 263. Iqbal, M., Ashraf, M., 2010. Changes in hormonal balance: a possible mechanism of pre-sowing chilling-induced salt tolerance in spring wheat. J. Agron. Crop Sci. 196, 440 454. Iqbal, U., Jamil, N., Ali, I., Hasnain, S., 2010. Effect of zinc-phosphate-solubilizing bacterial isolates on growth of Vigna radiata. Ann. Microbiol. 60, 243 248. Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K., Barea, J.-M., 2003. The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol. Fertil. Soils 37, 1 16. Jha, Y., Subramanian, R.B., Patel, S., 2011. Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol. Plant. 33, 797 802. Jiang, F., Chen, L., Belimov, A.A., Shaposhnikov, A.I., Gong, F., Meng, X., et al., 2012. Multiple impacts of the plant growth-promoting rhizobacterium Variovorax paradoxus 5C-2 on nutrient and ABA relations of Pisum sativum. J. Exp. Bot. 63, 6421 6430.

Plant Life under Changing Environment

References

389

Jin, C.W., He, Y.F., Tang, C.X., Wu, P., Zheng, S.J., 2006. Mechanisms of microbially enhanced Fe acquisition in red clover (Trifolium pratense L.). Plant Cell Environ. 29, 888 897. Kamran, M.A., Mufti, R., Mubariz, N., Syed, J.H., Bano, A., Javed, M.T., et al., 2014. The potential of the flora from different regions of Pakistan in phytoremediation: a review. Environ. Sci. Pollut. Res. 21, 801 812. Kang, S.-M., Khan, A.L., Waqas, M., You, Y.-H., Kim, J.-H., Kim, J.-G., et al., 2014a. Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J. Plant Interact. 9, 673 682. Kang, S.-M., Radhakrishnan, R., Khan, A.L., Kim, M.-J., Park, J.-M., Kim, B.-R., et al., 2014b. Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol. Biochem. 84, 115 124. Kaushal, M., Wani, S.P., 2016a. Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann. Microbiol. 66, 35 42. Kaushal, M., Wani, S.P., 2016b. Rhizobacterial-plant interactions: strategies ensuring plant growth promotion under drought and salinity stress. Agric. Ecosyst. Environ. 231, 68 78. ´ vila, L.A., Visconti, A., et al., 2013. Screening of Kavamura, V.N., Santos, S.N., da Silva, J.L., Parma, M.M., A Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol. Res. 168, 183 191. Kavita, B., Shukla, S., Kumar, G.N., Archana, G., 2008. Amelioration of phytotoxic effects of Cd on mung bean seedlings by gluconic acid secreting rhizobacterium Enterobacter asburiae PSI3 and implication of role of organic acid. World J. Microbiol. Biotechnol. 24, 2965 2972. Khalid, A., Arshad, M., Zahir, Z.A., 2004. Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J. Appl. Microbiol. 96, 473 480. Khan, M.S., Zaidi, A., Wani, P.A., 2007. Role of phosphate-solubilizing microorganisms in sustainable agriculture—a review. Agron. Sustain. Dev. 27, 29 43. Khoshgoftarmanesh, A.H., Schulin, R., Chaney, R.L., Daneshbakhsh, B., Afyuni, M., 2010. Micronutrient-efficient genotypes for crop yield and nutritional quality in sustainable agriculture. A review. Agron. Sustain. Dev. 30, 83 107. Kim, K., Jang, Y.-J., Lee, S.-M., Oh, B.-T., Chae, J.-C., Lee, K.-J., 2014. Alleviation of salt stress by Enterobacter sp. EJ01 in tomato and Arabidopsis is accompanied by up-regulation of conserved salinity responsive factors in plants. Mol. Cells 37, 109. Kim, S.-Y., Lim, J.-H., Park, M.-R., Kim, Y.-J., Park, T.-I., Seo, Y.-W., et al., 2005. Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. BMB Rep. 38, 218 224. Kohler, J., Caravaca, F., Carrasco, L., Roldan, A., 2006. Contribution of Pseudomonas mendocina and Glomus intraradices to aggregate stabilization and promotion of biological fertility in rhizosphere soil of lettuce plants under field conditions. Soil Use Manage. 22, 298 304. Kohler, J., Herna´ndez, J.A., Caravaca, F., Rolda´n, A., 2009. Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ. Exp. Bot. 65, 245 252. Kumar, A., Prakash, A., Johri, B.N., 2011. Bacillus as PGPR in crop ecosystem. Bacteria in Agrobiology: Crop Ecosystems. Springer, pp. 37 59. Lamosa, P., Martins, L.O., Da Costa, M.S., Santos, H., 1998. Effects of temperature, salinity, and medium composition on compatible solute accumulation by Thermococcus spp. Appl. Environ. Microbiol. 64, 3591 3598. Larpin, S., Sauvageot, N., Pichereau, V., Laplace, J.-M., Auffray, Y., 2002. Biosynthesis of exopolysaccharide by a Bacillus licheniformis strain isolated from ropy cider. Int. J. Food Microbiol. 77, 1 9. Latef, A.A.H.A., Miransari, M., 2014. The role of arbuscular mycorrhizal fungi in alleviation of salt stress. Use of Microbes for the Alleviation of Soil Stresses. Springer, pp. 23 38. Latour, X., Delorme, S., Mirleau, P., Lemanceau, P., 2009. Identification of traits implicated in the rhizosphere competence of fluorescent pseudomonads: description of a strategy based on population and model strain studies. Sustainable Agriculture. Springer, pp. 285 296. Ledger, T., Rojas, S., Timmermann, T., Pinedo, I., Poupin, M.J., Garrido, T., et al., 2016. Volatile-mediated effects predominate in Paraburkholderia phytofirmans growth promotion and salt stress tolerance of Arabidopsis thaliana. Front. Microbiol. 7, 1838. Leifert, C., Waites, W.M., Nicholas, J.R., 1989. Bacterial contaminants of micropropagated plant cultures. J. Appl. Bacteriol. 67, 353 361.

Plant Life under Changing Environment

390

15. Plant microbe interactions in plants and stress tolerance

Lim, J.-H., Kim, S.-D., 2013. Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol. J. 29, 201. Liu, F., Xing, S., Ma, H., Du, Z., Ma, B., 2013. Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl. Microbiol. Biotechnol. 97, 9155 9164. Liu, P., Yin, L., Wang, S., Zhang, M., Deng, X., Zhang, S., et al., 2015. Enhanced root hydraulic conductance by aquaporin regulation accounts for silicon alleviated salt-induced osmotic stress in Sorghum bicolor L. Environ. Exp. Bot. 111, 42 51. Loaces, I., Ferrando, L., Scavino, A.F., 2011. Dynamics, diversity and function of endophytic siderophoreproducing bacteria in rice. Microb. Ecol. 61, 606 618. Lugtenberg, B., 2015. Life of microbes in the rhizosphere. In: Lugtenberg, B. (Ed.), Principles of Plant-Microbe Interactions: Microbes for Sustainable Agriculture. Springer International Publishing, Cham, pp. 7 15. Lugtenberg, B., Kamilova, F., 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541 556. Lugtenberg, B.J.J., Malfanova, N., Kamilova, F., Berg, G., 2013. Plant growth promotion by microbes. Mol. Microb. Ecol. Rhizosph. vols. 1 and 2, 559 573. Ma, Y., Rajkumar, M., Luo, Y., Freitas, H., 2011. Inoculation of endophytic bacteria on host and non-host plants— effects on plant growth and Ni uptake. J. Hazard. Mater. 195, 230 237. Madhaiyan, M., Poonguzhali, S., Sa, T., 2007. Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69, 220 228. Mahajan, S., Tuteja, N., 2005. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139 158. Malusa´, E., Sas-Paszt, L., Ciesielska, J., 2012. Technologies for beneficial microorganisms inocula used as biofertilizers. Sci. World J. 2012, 491206. Manter, D.K., Delgado, J.A., Holm, D.G., Stong, R.A., 2010. Pyrosequencing reveals a highly diverse and cultivarspecific bacterial endophyte community in potato roots. Microb. Ecol. 60, 157 166. Marques, A.P.G.C., Moreira, H., Franco, A.R., Rangel, A.O.S.S., Castro, P.M.L., 2013. Inoculating Helianthus annuus (sunflower) grown in zinc and cadmium contaminated soils with plant growth promoting bacteria—effects on phytoremediation strategies. Chemosphere 92, 74 83. Martinez, C., 2010. Sustainable development and biodiversity. Environ. Policy Law 40, 273. Martı´nez-Gil, M., Ramos-Gonza´lez, M.I., Espinosa-Urgel, M., 2014. Roles of cyclic di-GMP and the Gac system in transcriptional control of the genes coding for the Pseudomonas putida adhesins LapA and LapF. J. Bacteriol. 196, 1484 1495. Marulanda, A., Barea, J.-M., Azco´n, R., 2009. Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J. Plant Growth Regul. 28, 115 124. Marulanda, A., Azco´n, R., Chaumont, F., Ruiz-Lozano, J.M., Aroca, R., 2010. Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232, 533 543. Matusik, J., Bajda, T., Manecki, M., 2008. Immobilization of aqueous cadmium by addition of phosphates. J. Hazard. Mater. 152, 1332 1339. Mayak, S., Tirosh, T., Glick, B.R., 2004. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci. 166, 525 530. Meena, V.S., Maurya, B.R., Verma, J.P., 2014. Does a rhizospheric microorganism enhance K 1 availability in agricultural soils? Microbiol. Res. 169, 337 347. Meena, V.S., Maurya, B.R., Verma, J.P., Meena, R.S., 2016. Potassium Solubilizing Microorganisms for Sustainable Agriculture. Springer. Miller, G.A.D., Suzuki, N., Ciftci-Yilmaz, S., Mittler, R.O.N., 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 33, 453 467. Miransari, M., 2011. Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol. Adv. 29, 645 653. Miransari, M., 2013. Soil microbes and the availability of soil nutrients. Acta Physiol. Plant. 35, 3075 3084. Mittova, V., Tal, M., Volokita, M., Guy, M., 2003. Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ. 26, 845 856.

Plant Life under Changing Environment

References

391

Moshelion, M., Halperin, O., Wallach, R., Oren, R.A.M., Way, D.A., 2015. Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield. Plant Cell Environ. 38, 1785 1793. Mus, F., Crook, M.B., Garcia, K., Garcia Costas, A., Geddes, B.A., Kouri, E.D., et al., 2016. Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl. Environ. Microbiol. 82, 3698. Nabti, E., Sahnoune, M., Ghoul, M., Fischer, D., Hofmann, A., Rothballer, M., et al., 2010. Restoration of growth of durum wheat (Triticum durum var. waha) under saline conditions due to inoculation with the rhizosphere bacterium Azospirillum brasilense NH and extracts of the marine alga Ulva lactuca. J. Plant Growth Regul. 29, 6 22. Nadeem, S.M., Zahir, Z.A., Naveed, M., Arshad, M., 2009. Rhizobacteria containing ACC-deaminase confer salt tolerance in maize grown on salt-affected fields. Can. J. Microbiol. 55, 1302 1309. Nadeem, S.M., Zahir, Z.A., Naveed, M., Nawaz, S., 2013. Mitigation of salinity-induced negative impact on the growth and yield of wheat by plant growth-promoting rhizobacteria in naturally saline conditions. Ann. Microbiol. 63, 225 232. Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8, 199 216. Naseem, H., Bano, A., 2014. Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. J. Plant Interact. 9, 689 701. Nautiyal, C.S., Srivastava, S., Chauhan, P.S., Seem, K., Mishra, A., Sopory, S.K., 2013. Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol. Biochem. 66, 1 9. Naveed, M., Mitter, B., Reichenauer, T.G., Wieczorek, K., Sessitsch, A., 2014. Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ. Exp. Bot. 97, 30 39. Nocker, A., Ferna´ndez, P.S., Montijn, R., Schuren, F., 2012. Effect of air drying on bacterial viability: a multiparameter viability assessment. J. Microbiol. Methods 90, 86 95. Noll, M.R., 2003. Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals. J. Environ. Qual. 32, 374. Noori, F., Etesami, H., Najafi Zarini, H., Khoshkholgh-Sima, N.A., Hosseini Salekdeh, G., Alishahi, F., 2018. Mining alfalfa (Medicago sativa L.) nodules for salinity tolerant non-rhizobial bacteria to improve growth of alfalfa under salinity stress. Ecotoxicol. Environ. Saf. 162, 129 138. Ogut, M., Er, F., Kandemir, N., 2010. Phosphate solubilization potentials of soil Acinetobacter strains. Biol. Fertil. Soils 46, 707 715. Olanrewaju, O.S., Glick, B.R., Babalola, O.O., 2017. Mechanisms of action of plant growth promoting bacteria. World J. Microbiol. Biotechnol. 33, 197. Omar, S.A., 1997. The role of rock-phosphate-solubilizing fungi and vesicular arbusular-mycorrhiza (VAM) in growth of wheat plants fertilized with rock phosphate. World J. Microbiol. Biotechnol. 14, 211 218. Ortiz, N., Armada, E., Duque, E., Rolda´n, A., Azco´n, R., 2015. Contribution of arbuscular mycorrhizal fungi and/ or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J. Plant Physiol. 174, 87 96. Ortı´z-Castro, R., Contreras-Cornejo, H.A., Macı´as-Rodrı´guez, L., Lo´pez-Bucio, J., 2009. The role of microbial signals in plant growth and development. Plant Signaling Behav. 4, 701 712. Osakabe, Y., Osakabe, K., Shinozaki, K., Tran, L.-S.P., 2014. Response of plants to water stress. Front. Plant Sci. 5, 86. Osorio Vega, N.W., 2007. A review on beneficial effects of rhizosphere bacteria on soil nutrient availability and plant nutrient uptake. Rev. Facul. Nacional Agron. Med. 60, 3621 3643. Ozanne, P.G., 1980. Phosphate Nutrition of Plants—A General Treatise. In: Khasawneh, F.E., Sample, E.C., Kamprath, E.J., (Eds.), The role of phosphorus in agriculture. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison, WI, pp. 559 589. Pacwa-Płociniczak, M., Płaza, G.A., Piotrowska-Seget, Z., Cameotra, S.S., 2011. Environmental applications of biosurfactants: recent advances. Int. J. Mol. Sci. 12, 633 654. Park, J., Bolan, N., Megharaj, M., Naidu, R., 2010. Isolation of phosphate-solubilizing bacteria and characterization of their effects on lead immobilization (,special issue. international symposium: challenges to soil degradation towards sustaining life and environment, Tokyo Metropolitan University symposium series no. 2, 2009). Pedologist 53, 67 75.

Plant Life under Changing Environment

392

15. Plant microbe interactions in plants and stress tolerance

Parmar, P., 2010. Isolation of Potassium Solubilizing Bacteria and Their Inoculation Effect on Growth of Wheat (Triticum aestivum L. em. Thell.) M.Sc. thesis submitted to CCS Haryana Agricultural University, Hisar. Parmar, P., Sindhu, S.S., 2013. Potassium solubilization by rhizosphere bacteria: influence of nutritional and environmental conditions. J. Microbiol. Res. 3, 25 31. Patel, K.J., Singh, A.K., Nareshkumar, G., Archana, G., 2010. Organic-acid-producing, phytate-mineralizing rhizobacteria and their effect on growth of pigeon pea (Cajanus cajan). Appl. Soil Ecol. 44, 252 261. Paul, E.A., 2007. Soil Microbiology and Biochemistry, third ed. Linacre House, Jordan Hill, Oxford. Paul, D., Sarma, Y.R., 2006. Plant growth promoting rhizhobacteria (PGPR)-mediated root proliferation in black pepper (Piper nigrum L.) as evidenced through GS root software. Arch. Phytopathol. Plant Prot. 39, 311 314. Paul, D., Nair, S., 2008. Stress adaptations in a plant growth promoting rhizobacterium (PGPR) with increasing salinity in the coastal agricultural soils. J. Basic Microbiol. 48, 378 384. Paul, D., Lade, H., 2014. Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron. Sustain. Dev. 34, 737 752. Pereyra, M.A., Garcia, P., Colabelli, M.N., Barassi, C.A., Creus, C.M., 2012. A better water status in wheat seedlings induced by Azospirillum under osmotic stress is related to morphological changes in xylem vessels of the coleoptile. Appl. Soil Ecol. 53, 94 97. Perez, E., Sulbaran, M., Ball, M.M., Yarzabal, L.A., 2007. Isolation and characterization of mineral phosphatesolubilizing bacteria naturally colonizing a limonitic crust in the south-eastern Venezuelan region. Soil Biol. Biochem. 39, 2905 2914. Podile, A.R., Kishore, G.K., 2006. Plant growth-promoting rhizobacteria. In: Gnanamanickam, S.S. (Ed.), PlantAssociated Bacteria. Springer, Amsterdam, The Netherlands, pp. 195 230. Pompelli, M.F., Barata-Luı´s, R., Vitorino, H.S., Gonc¸alves, E.R., Rolim, E.V., Santos, M.G., et al., 2010. Photosynthesis, photoprotection and antioxidant activity of purging nut under drought deficit and recovery. Biomass Bioenergy 34, 1207 1215. Porcel, R., Aroca, R., Ruiz-Lozano, J.M., 2012. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev. 32, 181 200. Qin, Y., Druzhinina, I.S., Pan, X., Yuan, Z., 2016. Microbially mediated plant salt tolerance and microbiome-based solutions for saline agriculture. Biotechnol. Adv. 34, 1245 1259. Qiu, Q., Wang, Y., Yang, Z., Yuan, J., 2011. Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L.) cultivars differing in cadmium accumulation. Food Chem. Toxicol. 49, 2260 2267. Qurashi, A.W., Sabri, A.N., 2012. Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz. J. Microbiol. 43, 1183 1191. Rajkumar, M., Ae, N., Prasad, M.N., Freitas, H., 2010a. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28, 142 149. Rajkumar, M., Ae, N., Prasad, M.N.V., Freitas, H., 2010b. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28, 142 149. Rajkumar, M., Ma, Y., Freitas, H., 2013. Improvement of Ni phytostabilization by inoculation of Ni resistant Bacillus megaterium SR28C. J. Environ. Manage. 128, 973 980. Ramos-Solano, B., Lucas Garcı´a, J.A., Garcia-Villaraco, A., Algar, E., Garcia-Cristobal, J., Gutierrez Man˜ero, F.J., 2010. Siderophore and chitinase producing isolates from the rhizosphere of Nicotiana glauca Graham enhance growth and induce systemic resistance in Solanum lycopersicum L. Plant Soil 334, 189 197. Rapparini, F., Pen˜uelas, J., 2014. Mycorrhizal fungi to alleviate drought stress on plant growth, Use of Microbes for the Alleviation of Soil Stresses, vol. 1. Springer, pp. 21 42. Rashid, M., Khalil, S., Ayub, N., Alam, S., Latif, F., 2004. Organic acids production and phosphate solubilization by phosphate solubilizing microorganisms (PSM) under in vitro conditions. Pak. J. Biol. Sci. 7, 187 196. Richardson, A.E., Simpson, R.J., 2011. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol. 156, 989 996. Roberson, E.B., Firestone, M.K., 1992. Relationship between desiccation and exopolysaccharide production in a soil Pseudomonas sp. Appl. Environ. Microbiol. 58, 1284 1291. Rodrı´guez-Salazar, J., Sua´rez, R., Caballero-Mellado, J., Iturriaga, G., 2009. Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol. Lett. 296, 52 59.

Plant Life under Changing Environment

References

393

Rodrı´guez, H., Fraga, R., 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17, 319 339. Rojas-Tapias, D., Moreno-Galva´n, A., Pardo-Dı´az, S., Obando, M., Rivera, D., Bonilla, R., 2012. Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Appl. Soil Ecol. 61, 264 272. Rolli, E., Marasco, R., Vigani, G., Ettoumi, B., Mapelli, F., Deangelis, M.L., et al., 2015. Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ. Microbiol. 17, 316 331. Ryu, C.-M., Farag, M.A., Hu, C.-H., Reddy, M.S., Kloepper, J.W., Pare´, P.W., 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134, 1017 1026. Saber, M.S.M., Zanati, M.R., 1984. Effectiveness of inoculation with silicate bacteria in relation to the potassium content of plants using the intensive cropping technique. Agric. Res. Rev. 58, 279 293. Sadeghi, A., Karimi, E., Dahaji, P.A., Javid, M.G., Dalvand, Y., Askari, H., 2012. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J. Microbiol. Biotechnol. 28, 1503 1509. Safronova, V.I., Stepanok, V.V., Engqvist, G.L., Alekseyev, Y.V., Belimov, A.A., 2006. Root-associated bacteria containing 1-aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol. Fertil. Soils 42, 267 272. Sandhya, V., Ali, S.Z., 2015. He production of exopolysaccharide by Pseudomonas putida GAP-P45 under various abiotic stress conditions and its role in soil aggregation. Microbiology 84, 512 519. Sandhya, V., Grover, M., Reddy, G., Venkateswarlu, B., 2009. Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol. Fertil. Soils 46, 17 26. Sandhya, V., Ali, S.Z., Grover, M., Reddy, G., Venkateswarlu, B., 2010. Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul. 62, 21-30. Santi, C., Bogusz, D., Franche, C., 2013. Biological nitrogen fixation in non-legume plants. Ann. Bot. 111, 743 767. Saravanakumar, D., Samiyappan, R., 2007. ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J. Appl. Microbiol. 102, 1283 1292. Saravanan, V.S., Madhaiyan, M., Thangaraju, M., 2007. Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66, 1794 1798. Saravanan, V.S., Kumar, M.R., Sa, T.M., 2011. Microbial zinc solubilization and their role on plants. Bacteria in Agrobiology: Plant Nutrient Management. Springer, pp. 47 63. Sarma, B.K., Yadav, S.K., Singh, D.P., Singh, H.B., 2012. Rhizobacteria mediated induced systemic tolerance in plants: prospects for abiotic stress management. Bacteria in Agrobiology: Stress Management. Springer, pp. 225 238. Sarma, R.K., Saikia, R., 2014. Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant Soil 377, 111 126. Serraj, R., Sinclair, T., 2002. Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ. 25, 333 341. Sessitsch, A., Kuffner, M., Kidd, P., Vangronsveld, J., Wenzel, W.W., Fallmann, K., et al., 2013. The role of plantassociated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol. Biochem. 60, 182 194. Sgherri, C.L.M., Maffei, M., Navari-Izzo, F., 2000. Antioxidative enzymes in wheat subjected to increasing water deficit and rewatering. J. Plant Physiol. 157, 273 279. Sharma, R.K., Archana, G., 2016. Cadmium minimization in food crops by cadmium resistant plant growth promoting rhizobacteria. Appl. Soil Ecol. 107, 66 78. Sharma, S.B., Sayyed, R.Z., Trivedi, M.H., Gobi, T.A., 2013. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2, 587. Sharpley, A., Meisinger, J., Power, J., Suarez, D., 1992. Root extraction of nutrients associated with long-term soil management. Limitations to Plant Root Growth. Springer, pp. 151 217. Shrivastava, P., Kumar, R., 2015. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 22, 123 131.

Plant Life under Changing Environment

394

15. Plant microbe interactions in plants and stress tolerance

Siddikee, M.A., Chauhan, P.S., Anandham, R., Han, G.-H., Sa, T., 2010. Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J. Microbiol. Biotechnol. 20, 1577 1584. Sindhu, S.S., Parmar, P., Phour, M., Sehrawat, A., 2016. Potassium-Solubilizing Microorganisms (KSMs) and Its Effect on Plant Growth Improvement, Potassium Solubilizing Microorganisms for Sustainable Agriculture. Springer, pp. 171 185. Singh, L.P., Gill, S.S., Tuteja, N., 2011. Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signaling Behav. 6, 175 191. Singh, R.P., Jha, P.N., 2016. Alleviation of salinity-induced damage on wheat plant by an ACC deaminaseproducing halophilic bacterium Serratia sp. SL-12 isolated from a salt lake. Symbiosis 69, 101 111. Siripornadulsil, S., Siripornadulsil, W., 2013. Cadmium-tolerant bacteria reduce the uptake of cadmium in rice: potential for microbial bioremediation. Ecotoxicol. Environ. Saf. 94, 94 103. Somers, E., Vanderleyden, J., Srinivasan, M., 2008. Rhizosphere bacterial signalling: a love parade beneath our feet. Crit. Rev. Microbiol. 30 (4), 205 240. Sparks, D.L., Huang, P.M., 1985. Physical chemistry of soil potassium. Potassium in Agriculture. American Society of Agronomy, Madison, WI, pp. 201 276. Stamford, N.P., Santos, P.Rd, Moura, A.M.M.Fd, Freitas, A.D.Sd, 2003. Biofertilzers with natural phosphate, sulphur and Acidithiobacillus in a siol with low available-P. Sci. Agric. 60, 767 773. Sturz, A.V., Christie, B.R., Nowak, J., 2000. Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit. Rev. Plant Sci. 19, 1 30. Sua´rez, R., Wong, A., Ramı´rez, M., et al., 2008. Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol. Plant-Microbe Interact. 21, 958 966. Sun, X., Guo, L., 2013. Relationship between cadmium-induced root subapical hair development and ethylene biosynthesis in oilseed rape seedlings. Acta Biol. Cracoviensia Series Botanica 55, 68 75. Susilowati, L.E., Syekhfani, S., 2014. Characterization of phosphate solubilizing bacteria isolated from Pb contaminated soils and their potential for dissolving tricalcium phosphate. J. Degraded Min. Lands Manage. 1, 57 62. Syers, J.K., Johnston, A.E., Curtin, D., 2008. Efficiency of soil and fertilizer phosphorus use. FAO Fertilizer and Plant Nutrition Bulletin. Food and Agriculture Organization of the United Nations (FAO), Rome, p. 18. Sziderics, A.H., Rasche, F., Trognitz, F., Sessitsch, A., Wilhelm, E., 2007. Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can. J. Microbiol. 53, 1195 1202. Tank, N., Saraf, M., 2010. Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J. Plant Interact. 5, 51 58. Tewari, S., Arora, N.K., 2014. Multifunctional exopolysaccharides from Pseudomonas aeruginosa PF23 involved in plant growth stimulation, biocontrol and stress amelioration in sunflower under saline conditions. Curr. Microbiol. 69, 484 494. Theunis, M., 2005. IAA Biosynthesis in Rhizobia and Its Potential Role in Symbiosis (Ph.D. thesis). Universiteit Antwerpen. Thrall, P.H., Hochberg, M.E., Burdon, J.J., Bever, J.D., 2007. Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol. Evol. 22, 120 126. Timmusk, S., El-Daim, I.A.A., Copolovici, L., Tanilas, T., Ka¨nnaste, A., Behers, L., et al., 2014. Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9, e96086. Tisdale, S.L., Nelson, W.L., Beaton, J.D., 1985. Soil Fertility and Fertilizers. Collier Macmillan Publishers. Uchida, R., 2000. Essential nutrients for plant growth: nutrient functions and deficiency symptoms. Plant Nutrient Management in Hawaii’s Soils. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa, pp. 31 55. Upadhyay, S., Singh, J., Singh, D., 2011. Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere 21, 214 222. Upadhyay, S.K., Singh, D.P., 2015. Effect of salt-tolerant plant growth-promoting rhizobacteria on wheat plants and soil health in a saline environment. Plant Biol. 17, 288 293. Upadhyay, S.K., Singh, J.S., Saxena, A.K., Singh, D.P., 2012. Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol. 14, 605 611.

Plant Life under Changing Environment

References

395

Uroz, S., Calvaruso, C., Turpault, M.-P., Frey-Klett, P., 2009. Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol. 17, 378 387. Vaishnav, A., Kumari, S., Jain, S., Varma, A., Choudhary, D.K., 2015. Putative bacterial volatile-mediated growth in soybean (Glycine max L. Merrill) and expression of induced proteins under salt stress. J. Appl. Microbiol. 119, 539 551. Van Loon, L.C., Bakker, P., Pieterse, C.M.J., 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36, 453 483. Vardharajula, S., Zulfikar Ali, S., Grover, M., Reddy, G., Bandi, V., 2011. Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J. Plant Interact. 6, 1 14. Venkateswarlu, B., Shanker, A.K., 2009. Climate change and agriculture: adaptation and mitigation strategies. Indian J. Agron. 54, 226 230. Vinocur, B., Altman, A., 2005. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr. Opin. Biotechnol. 16, 123 132. Vu, B., Chen, M., Crawford, R.J., Ivanova, E.P., 2009. Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14, 2535 2554. Wagner, S.C., 2011. Biological nitrogen fixation. Nat. Educ. Knowl. 3 (10) 15. Wakelin, S.A., Warren, R.A., Harvey, P.R., Ryder, M.H., 2004. Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol. Fertil. Soils 40, 36 43. Wang, C., Knill, E., Glick, B.R., De´fago, G., 2000. Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gac A derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can. J. Microbiol. 46, 898 907. Wang, C.-J., Yang, W., Wang, C., Gu, C., Niu, D.-D., Liu, H.-X., et al., 2012. Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 7, e52565. Wang, Q., Dodd, I.C., Belimov, A.A., Jiang, F., 2016a. Rhizosphere bacteria containing 1-aminocyclopropane-1carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na 1 accumulation. Funct. Plant Biol. 43, 161 172. Wang, S., Wang, F., Gao, S., Wang, X., 2016b. Heavy metal accumulation in different rice cultivars as influenced by foliar application of nano-silicon. Water Air Soil Pollut. 227, 1 13. Wang, Y., Ohara, Y., Nakayashiki, H., Tosa, Y., Mayama, S., 2005. Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol. Plant-Microbe Interact. 18, 385 396. Wei, X., Fang, L., Cai, P., Huang, Q., Chen, H., Liang, W., et al., 2011. Influence of extracellular polymeric substances (EPS) on Cd adsorption by bacteria. Environ. Pollut. 159, 1369 1374. Welch, R.M., Shuman, L., 1995. Micronutrient nutrition of plants. Crit. Rev. Plant Sci. 14, 49 82. Welman, A.D., Maddox, I.S., 2003. Exopolysaccharides from lactic acid bacteria: perspectives and challenges. Trends Biotechnol. 21, 269 274. Whipps, J.M., 2001. Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52, 487 511. Wintermans, P.C.A., Bakker, P.A.H.M., Pieterse, C.M.J., 2016. Natural genetic variation in Arabidopsis for responsiveness to plant growth-promoting rhizobacteria. Plant Mol. Biol. 90, 623 634. Wu, H., Chen, C., Du, J., Liu, H., Cui, Y., Zhang, Y., et al., 2012. Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol. 158, 790 800. Xie, Z., Song, R., Shao, H., Song, F., Xu, H., Lu, Y., 2015. Silicon improves maize photosynthesis in saline-alkaline soils. Sci. World J. 2015, p. 245072. Xu, X., Huang, Q., Huang, Q., Chen, W., 2012. Soil microbial augmentation by an EGFP-tagged Pseudomonas putida X4 to reduce phytoavailable cadmium. Int. Biodeterior. Biodegrad. 71, 55 60. Yan, J., Smith, M.D., Glick, B.R., Liang, Y., 2014. Effects of ACC deaminase containing rhizobacteria on plant growth and expression of Toc GTPases in tomato (Solanum lycopersicum) under salt stress. Botany 92, 775 781. Yang, A., Akhtar, S.S., Iqbal, S., Amjad, M., Naveed, M., Zahir, Z.A., et al., 2016. Enhancing salt tolerance in quinoa by halotolerant bacterial inoculation. Funct. Plant Biol. 43, 632 642. Yang, J., Kloepper, J.W., Ryu, C.-M., 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14, 1 4.

Plant Life under Changing Environment

396

15. Plant microbe interactions in plants and stress tolerance

Yao, L., Wu, Z., Zheng, Y., Kaleem, I., Li, C., 2010. Growth promotion and protection against salt stress by Pseudomonas putida Rs-198 on cotton. Eur. J. Soil Biol. 46, 49 54. Yi, Y., Huang, W., Ge, Y., 2008. Exopolysaccharide: a novel important factor in the microbial dissolution of tricalcium phosphate. World J. Microbiol. Biotechnol. 24, 1059 1065. Yu, X., Li, Y., Zhang, C., Liu, H., Liu, J., Zheng, W., et al., 2014. Culturable heavy metal-resistant and plant growth promoting bacteria in V-Ti magnetite mine tailing soil from Panzhihua, China. PLoS One 9, e106618. Zahir, Z.A., Munir, A., Asghar, H.N., Shaharoona, B., Arshad, M., 2008. Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J. Microbiol. Biotechnol. 18, 958 963. Zarea, M., Hajinia, S., Karimi, N., Goltapeh, E.M., Rejali, F., Varma, A., 2012. Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol. Biochem. 45, 139 146. Zawoznik, M.S., Ameneiros, M., Benavides, M.P., Va´zquez, S., Groppa, M.D., 2011. Response to saline stress and aquaporin expression in Azospirillum-inoculated barley seedlings. Appl. Microbiol. Biotechnol. 90, 1389 1397. Zerrouk, I.Z., Benchabane, M., Khelifi, L., Yokawa, K., Ludwig-Mu¨ller, J., Baluska, F., 2016. A Pseudomonas strain isolated from date-palm rhizospheres improves root growth and promotes root formation in maize exposed to salt and aluminum stress. J. Plant Physiol. 191, 111 119. Zhang, H., Kim, M.-S., Sun, Y., Dowd, S.E., Shi, H., Pare´, P.W., 2008. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol. Plant-Microbe Interact. 21, 737 744. Zhu, J.-K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247. Zhuang, X., Chen, J., Shim, H., Bai, Z., 2007. New advances in plant growth-promoting rhizobacteria for bioremediation. Environ. Int. 33, 406 413. Zo¨rb, C., Senbayram, M., Peiter, E., 2014. Potassium in agriculture status and perspectives. J. Plant Physiol. 171, 656 669. Zou, C.-S., Mo, M.-H., Gu, Y.-Q., Zhou, J.-P., Zhang, K.-Q., 2007. Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol. Biochem. 39, 2371 2379. Zushi, K., Matsuzoe, N., Kitano, M., 2009. Developmental and tissue-specific changes in oxidative parameters and antioxidant systems in tomato fruits grown under salt stress. Sci. Hortic. 122, 362 368. Złoch, M., Thiem, D., Gadzała-Kopciuch, R., Hrynkiewicz, K., 2016. Synthesis of siderophores by plant-associated metallotolerant bacteria under exposure to Cd2 1 . Chemosphere 156, 312 325.

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16 Phytohormonal signaling under abiotic stress Zahra Souri1, Naser Karimi1, Muhammad Ansar Farooq2 and Javaid Akhtar2 1

Laboratory of Plant Physiology, Department of Biology, Faculty of Science, Razi University, Kermanshah, Iran 2Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan

16.1 Introduction Plants, as sessile organisms, live in constantly changing environments that are often unfavorable or stressful for plants in terms of growth and development. Since growth and productivity of plants are limited by numerous types of abiotic stresses (e.g., drought, salt stress, and extreme temperature) and chemical factors, such as metal or metalloid stress, plants respond to such growth adversities via efficient defense-response mechanisms, including activation of various stress-responsive genes that help them in the maintenance of cellular homeostasis under such marginal growth conditions (Knight and Knight, 2001; Qin et al., 2011b). Plants prompt a well-coordinated and inimitable molecular response at cellular level after exposure to stressful growth conditions in order to minimize the damage and ensure survival (Fahad et al., 2015a,b). Exposure of plants to multiple abiotic stress conditions causes a variety of metabolic, biochemical, physiological and molecular alterations, subsequently causing oxidative damage and interfering with the normal metabolic activities and ultimately yield decline (Xiong and Zhu, 2002; Basu and Rabara, 2017). A well-coordinated and timely response to such stresses involves signal perception and transduction mainly via plant hormones, that is, phytohormones. Phytohormones comprises a wide array of signaling compounds present in minute quantities in cells, playing crucial roles in stimulating plant acclimation to environmental stresses by facilitating growth and developmental processes, transitions of sink/source, and also coordinating various pathways of signal transduction during stress responses (Fahad et al., 2015b,c; Wani et al., 2016). The timely perception of the stress signal is a crucial step in plant

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00019-9

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16. Phytohormonal signaling under abiotic stress

defense. The fundamental defense response leads to the stimulation of signaling events of in a stress-dependent manner (Chinnusamy et al., 2004; Rejeb et al., 2014). Following stresses exposure, specific ionic channels and cascade events, for example, kinase cascades are stimulated, and ROS (reactive oxygen species) and phytohormones are accumulated. A reprogramming of the genetic machinery effects then in adequate defense responses and an enhancement in plant capability to tolerate the stress (Fraire-Vela´zquez et al., 2011; Rejeb et al., 2014; Verma et al., 2016). The elegant phytohormone signaling networks and their interactions render them ideal candidates for mediating defense responses (Verma et al., 2016). Abiotic stresses, for example, drought and salt stress, cause reduced soil water availability, which lead plants to decrease turgor pressure, causing osmotic stress and promoting the synthesis of phytohormones (Danquah et al., 2014; Basu and Rabara, 2017; Vishwakarma et al., 2017). The main classes of phytohormones include (1) classical phytohormones such as auxin (AUX), abscisic acid (ABA), brassinosteroids (BRs), ethylene (ET), gibberellins (GAs), and cytokinin (CK); (2) molecular phytohormones, for example, jasmonic acid (JA), salicylic acid (SA), and nitric oxide (NO); and (3) newly discovered karrikins (KARs) and strigolactones (SLs) (Fig. 16.1) (Smith and Li, 2014; Pandey et al., 2016). Phytohormones, also named as plant growth regulators, are signaling molecules resulting from plant biosynthetic paths that might act either locally or be transported to another location in the plant to induce responses of growth and developmental responses under stressful conditions (Peleg and Blumwald, 2011; Fahad et al., 2015b). All the phases of the plant cell life are regulated by the action of many phytohormones, which control several biochemical and physiological processes (Iqbal et al., 2014). Moreover, phytohormones are vital for the plant’s ability to withstand abiotic stresses by arbitrating a wide array of stress

BRs

ET

GAs

JA

SA

NO

New phytohormones

AUX

Molecular phytohormones

Classical phytohormones

ABA

SLs

KARs

CK

FIGURE 16.1 The phytohormones that are categorized into three groups: classical phytohormones (ABA, AUX, BRs, ET, Gas, CK), molecular phytohormones (JA, SA, and NO), and new class of phytohormones (SLs and KARs). ABA, Abscisic acid; AUX, auxin; BRs, brassinosteroids; CK, cytokinin; ET, ethylene; JA, jasmonic acid; KARs, karrikins; SA, salicylic acid; SLs, strigolactones.

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responses, which take place via numerous signal transduction networks including transcription factors (TFs) regulating phytohormones signaling (Wang and Irving, 2011; Khan et al., 2012c). Since, knowledge about the function of phytohormones on abiotic stresses is partial, in this chapter, we give a perspective of the phytohormones and their vital roles in cell signaling and link this process to plant stress tolerance.

16.2 Abscisic acid During a plant’s life cycle, ABA is reported to be endogenously produced messenger to control various biochemical and physiological processes, for example, embryo morphogenesis, seed development and dormancy, stomatal closure, storage proteins and lipids synthesis, and organ senescence. It is also closely correlated to increased plant tolerance against various abiotic stresses (Tuteja, 2007; Tuteja and Sopory, 2008; Danquah et al., 2014; Vishwakarma et al., 2017). At the membrane level, the signal of stress is first perceived by the receptors localized on cell membranes such as histidine kinase (HK), receptor-like kinase (RLK), or ion-channel leading to the activation of a multifaceted signaling cascade, including the production of secondary messengers such as calcium (Ca21), ROS, inositol phosphates (InsP), and ABA (Tuteja, 2007; Tripathy and Oelmu¨ller, 2012). Next, activated signals persuade numerous stress-responsive genes, resulting ultimately in the plant acclimation response (Tuteja, 2007; Tuteja and Sopory, 2008). Under water deficit, appropriate response is initiated with the discernment of osmotic signals via several receptors of membrane such as G-protein-coupled receptors, RLKs, ion channels, HKs and changing cytoplasmic levels of Ca21, and generating secondary signaling molecules (InsP, ROS, and ABA), which initiate a protein phosphorylation cascade by various kinases such as CBL-interacting protein kinases, calcium-dependent protein kinases (CDPKs), and other kinases and phosphatases (Kim et al., 2010; Verma et al., 2016). In addition, there is a significant role of MAPK-induced pathway in ABA signal transduction pathways, involving antioxidant defense responses and guard cell signaling (Zong et al., 2009; Danquah et al., 2014; Raja et al., 2017). These various kinases can modulate TFs through phosphorylation and dephosphorylation actions, and then these TFs are able to stimulate various stress-responsive genes, which include genes coding for HSPs (heat shock proteins), late embryogenesis abundant (LEA) proteins, antioxidants, osmolytes, and other genes linked to response to stresses (Yoshida et al., 2014; Verma et al., 2013, 2016). ABA is a key phytohormone playing vital role in acting toward a varied range of abiotic stresses, being commonly known as the “stress hormone” (Vishwakarma et al., 2017). The old root-sourced ABA theory, which stated that ABA is transported via xylem sap to the guard cells to promote stomatal closure (Davies and Zhang, 1991), has been very recently challenged by a number of studies demonstrating that foliar ABA, rather than the ones that are root-sourced, regulates stomata closure (Holbrook et al., 2002; McAdam et al., 2016; Zhang et al., 2018), where, by closing stomata, this phytohormone prevents a further decline in water potentials and contributes to the plant’s adaptation to various abiotic stresses (Wilkinson and Davies, 2002; Pantin et al., 2013; Bu¨cker-Neto et al., 2017).

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Generally, ABA action is able to mark explicitly the guard cells for the initiation of stomata closure, which, however, might also transduce cellular signals in a systematic way for readjustments under extreme drought and osmotic stress (Tuteja, 2007). ABA persuades the stomatal closure to decrease transpirational water loss, as well as alleviates biological damage by the stimulation of numerous stress-responsive genes encoding compatible osmolyte biosynthesis enzymes (Bray, 2002; Finkelstein et al., 2002; Xiong and Zhu, 2002; Sah et al., 2016; Joshi et al., 2016). Moreover, ABA was reported to counter balance the inhibitory influence of stress-induced ET on growth of plants and influencing the levels of ABA by altering the expression pattern of the key genes related to ABA biosynthesis and provide an impressive means to enhance the stress tolerance of plants (Sharp, 2002; Sah et al., 2016). There are various TFs to control the expression profile of ABA-responsive gene products, and stress-associated genes are able to express either by an ABA-dependent or ABAindependent manners (Chinnusamy et al., 2004; Tuteja, 2007). Indeed, the levels of ABA increase significantly under abiotic stresses that prompt the expression of numerous genes encoding various proteins (Finkelstein et al., 2002; Xiong et al., 2014). These proteins increase the ability of plants to tolerate the stresses and include LEAproteins and several enzymes of osmoprotectant biosynthesis pathways, decreasing oxidative damage, and signaling proteins/TFs, for example, AP2/ERF (Apetala2/ethylene response factor), bZIP, MYB, NAC (no apical meristem), and WRKY families that work as the early responders to environmental signals and prompt the activation of stress-induced gene products, which are essential for plant tolerance against numerous abiotic stresses (Zhang et al., 2006; Huang et al., 2012; Xiong et al., 2014; Basu and Rabara, 2017). During the recent years, it has been reported that the stimulation of TFs/signaling molecules in crop plant engineering is a powerful approach to enhance plant tolerance against stresses. For instance, the overexpression of AP3, OsbZIP23, OsbZIP46, and OsNAC10 in rice has been demonstrated to significantly improve rice tolerance in response to water shortage and salinity (Xiang et al., 2008; Oh et al., 2009; Jeong et al., 2010; Tang et al., 2012). Moreover, based on several studies, ABA levels in plant tissues is known to increase after heavy metal exposure, suggesting an involvement of this phytohormone in the induction of protective mechanisms against heavy metal toxicity. A transcriptome analysis has revealed strong expression of ABA biosynthesis genes OsNCED2 and OsNCED3, and also the upregulation of four ABA signaling genes upon heavy metal exposure (Poschenrieder et al., 1989; Fediuc et al., 2005; Huang et al., 2012; Kim et al., 2014; Wang et al., 2014; Bu¨cker-Neto et al, 2017).

16.3 Abscisic acid biosynthesis ABA is a sesquiterpene (C15H20O4), which originates from isopentenyl pyrophosphate (IPP), synthesized in plastids (Fig. 16.2). IPP is generated mainly in chloroplasts by 1deoxy-D-xylulose-5-phosphate from glyceraldehydes-3-phosphate and pyruvate, that leads to the stepwise generation of phytoene and β-carotene (Seo and Koshiba, 2002; Danquah et al., 2014). β-Carotene is changed to zeaxanthin and, in following steps, encompass the biosynthesis of cis-isomers of neoxanthin and violaxanthin which undergoes breakdown to synthesize xanthoxin, which is supposed to transfer from the plastid to the cytoplasm, where it is converted to ABA (Fig. 16.2) (Nambara and Marion-Poll, 2005).

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IPP Phytoene β-Carotene Zeaxanthin ZEP

Antheraxanthin ZEP

Violaxanthin

trans-Neoxanthin 9-cis-Violaxanthin

NCED

9-cis-Neoxanthin

AAO

SDR

Xanthoxin

ABA

Abscisic aldehyde

FIGURE 16.2

A schematic representation of the ABA biosynthesis pathway. ABA, Abscisic acid. Source: Modified from Tuteja, N., 2007. Abscisic acid and abiotic stress signaling. Plant Signal. Behav. 2, 135
138; Finkelstein, R., 2013. Abscisic acid synthesis and response. Arabidopsis Book 11, e0166; Sah, S.K., Reddy, K.R., Li, J., 2016. Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 7, 5714.

In plastids, the primary step specific to the pathway of ABA formation is the oxidative modification of antheraxanthin and zeaxanthin to violaxanthin, and this is stimulated by a zeaxanthin epoxidase (ZEP) (Fig. 16.2). In transgenic crops, it has been shown that the ZEP overexpression conferred enhanced tolerance against drought and salinity, demonstrating that this specific enzyme might be limited during few stress-responsive pathways (Park et al., 2008; Finkelstein, 2013). The breakdown of 9-cis-neoxanthin and 9-cis-violaxanthin is stimulated by the NCED (9-cis-epoxycarotenoid dioxygenase) enzymes, which is an important governing step for the synthesis of ABA (Fig. 16.2) (Iuchi et al., 2001; Qin and Zeevaart, 1999; Cai et al., 2015). In cytoplasm, xanthoxin is transformed to abscisic aldehyde by the short-chain dehydrogenase/reductase enzyme, and the last step for the synthesis of ABA is stimulated by AAO (abscisic aldehyde oxidase) (Fig. 16.2) (Finkelstein, 2013). The increase in de novo ABA biosynthesis is due to the increase in abiotic stress, which plays a role to inhibit its degradation and is supposed to be stimulated by stress alleviation (Vishwakarma et al., 2017). Under stress condition, the generation of ABA is induced,

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which is predominantly caused by the gene expression
encoding enzymes accountable for biosynthesis of ABA. These genes are including ZEP, NCED, AAO, and ABA3 (as a MoCo sulfurase) also identified as LOS5 (Xiong et al., 2001; Tuteja, 2007; Verma et al., 2016).

16.4 Abscisic acid signaling During ABA signaling, the primary events ensue through a fundamental signaling component comprised proteins associated to its three different classes: pyrabactin resistance/ pyrabactin resistance like/regulatory component of ABA receptor (PYR/PYL/RCARs) suggested as the ABA receptors, PP2Cs (protein phosphatase 2Cs), that negatively regulate, and subclass III sucrose nonfermenting1
related kinase2s (SNF1-related kinase2s or SnRK2s), which are stimulators (Schweighofer et al., 2004; Yoshida et al., 2006; Umezawa et al., 2010; Park et al., 2009; Danquah et al., 2014). The members of SnRK2 protein family are threonine specific to plants/serine-kinases tangled in stress responses, and the coordination of the plant response to ABA via SnRK2s-mediated pathway occurs via direct phosphorylation of numerous downstream targets, for example, SLAC1 (slow anion channel-associated 1), KAT1 (K1-inward rectifying channel), signaling molecules necessary for the expression of various stress-responsive genes (Fig. 16.3) (Santiago et al., 2012). It has also been introduced to two receptors, including GTG1/2 as a novel G-protein-coupled plasma membrane receptors class, which can interact with GPA1 to regulate ABA signaling (Luo et al., 2013). Recently, it has identified several ABA-responsive ZmPYLs and ZmSnRK2s, and also ZmPP2Cs by using Arabidopsis pyl112458 and snrk2.2/3/6 mutants (Wang et al., 2018). In general, ABA signal transduction under abiotic stress can be categorized into two manners: the ABA-dependent and ABA-independent (Fig. 16.3), and most of the basic genes in both manners have been studied, which are including TFs belonging to the class of ABA-binding factor (ABF), C-repeat-binding factor (CBF)/DRE-binding protein (DREB), MYB, and MYC (Cai et al., 2015). It has been indicated that, the further signaling molecules involved in ABA-induced or stress-induced expression response of genes, including the NAC, MYB, and MYC classes (Abe et al., 1997); WRKY factor; and HD-Zip (homeodomain leucine zipper) families (Rushton et al., 2012), are stimulated by ABA or abiotic stress (Finkelstein, 2013). MYB-type TFs, which are strongly induced by ABA, play important roles in the growth and developmental responses of plants against abiotic stresses (Xiong et al., 2014; Joshi et al., 2016). WRKY subclass encompass one of the largest families of TFs in plants, which participate in ABA signaling and stress responses, and they are able to increase drought tolerance and the regulation of ABA signal transduction pathways (Rushton et al., 2012; Chen et al., 2012b; Luo et al., 2013).

16.5 Abscisic acid
dependent signal transduction In ABA absence, PP2C negatively regulates SnRK2, whose autophosphorylation is necessary for activity of kinase toward downstream targets (Yang et al., 2017; Lee et al., 2013). The ABA binding via PYL/PYR/RCAR receptor promote the binding of the PP2C to

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16.5 Abscisic acid
dependent signal transduction

403

FIGURE 16.3 The ABA-dependent and ABA-independent signaling pathway in response to abiotic stress. In ABA signaling, PP2Cs, SnRK2s, and ABA-responsive elements binding factors (ABFs/AREBs), have key role. In the absence of ABA, PP2Cs inhibit protein kinase (SnRK2) activity, and in another side ABA is bound by intracellular PYR/PYL dimers, which dissociate to form ABA receptor
PP2C complexes. PP2Cs are key negative regulatory components of the ABA pathway involved in the dephosphorylation of SnRK2. AREB/ABF TFs regulate the ABRE-mediated transcription of downstream target genes, and SnRK2 phosphorylate and positively control the AREB/ABF TFs. PP2C-PYR/PYL/RCAR ABA receptor complex inhibits the activity of the PP2C in an ABAdependent manner, allowing activation of SnRK2s, which can phosphorylate downstream substrate proteins, including TFs and ion channels, thereby enhancing osmotic stress tolerance through inhibition of stomatal opening. ABA, Abscisic acid; ABF, ABA-binding factor; PP2Cs, Protein Phosphatase 2Cs; PYL, pyrabactin resistance like; PYR, pyrabactin resistance; RCARs, regulatory component of ABA receptor. Source: Modified from Yoshida, T., Mogami, J., Yamaguchi-Shinozaki, K., 2014. ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr. Opin. Plant Biol. 21, 133
139.

receptor, and this suppresses the activity of PP2C (Fig. 16.3), and in ABA presence, the subclass III SnRK2s (SRK2D/SnRK2.2, SRK2I/SnRK2.3, and SRK2E/SnRK2.6/OST1) mediated from PP2C-induced negatively regulated process of phosphorylate ABRE/ABFs (ABA-responsive element binding protein/binding factors), which in turn stimulate the expression pattern of several ABA-responsive transcripts (Fig. 16.3) (Hubbard et al., 2010; Weiner et al., 2010; Fujita et al., 2013; Vishwakarma et al., 2017). AREB/ABFs as bZIP TFs control transcription via binding to ABA-responsive complex, which is present in the promoter of the ABA inducible genes (Verma et al., 2013). Overexpression of ABF2/AREB1, ABF3, and ABF4/AREB2 as positive ABA signal

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regulators leads to the ABA-induced expression of genes (Verma et al., 2013; Yoshida et al., 2014). In transgenic plants, improve drought tolerance suggested that phosphorylation of AREB1 at multisite during ABA-dependent manner is important for its selfactivation (Verma et al., 2013; Yoshida et al., 2010, 2014). Indeed, in an ABA-dependent manner, AREB/ABF TFs are activated via multisite conserved domains phosphorylation by SnRK2s (Furihata et al., 2006; Yoshida et al., 2014). In Arabidopsis thaliana, nine out of ten SnRK2s are induced by osmotic-induced stress, with subclass III SnRK2s, SnRK2.2/SRK2D, SRK2I/SnRK2.3, and SRK2E/SnRK2.6/OST1 also intensely induced by ABA (Fujita et al., 2013; Yoshida et al., 2014, 2015). These SnRK2s interact with ABFs/AREB in nucleus, as well as activation of most downstream gene products of ABF2/AREB1, ABF3, and ABF4/AREB2 is considerably reduced in srk2d/e/i mutants, and ABA-dependent ABFs/AREB phosphorylation is fully reduced (Yoshida et al., 2006). These outcomes show that SnRK2s control the expression pattern of ABA-responsive genes via AREB/ABFs phosphorylation under stress condition, and phosphor
proteome analysis propose that ABFs/AREB are principal signaling molecules that function downstream of SnRK2s during ABA-induced signaling in osmotic stress response (Fujita et al., 2009; Yoshida et al., 2014, 2015). Recently, SNS1 (SNRK2-SUBSTRATE1) is recognized as a new substrate of SnRK2, but SNS1 is of unidentified function; further analysis is necessary to determine its detailed involvement in ABA-mediated signaling (Yoshida et al., 2015). The endogenously produced ABA levels are enhanced due to drought and salinity stress-induced osmotic stress, and ABA triggers the expression of many genes through ABREs present in promoter regions (Fujita et al., 2013; Sah et al., 2016; Vishwakarma et al., 2017). The phosphor
proteome analyses indicated that ABFs/AREB are the principal signaling molecules that function downstream of the subclass III SnRK2s during ABAinduced signaling under osmotic stress, and ABF1 is a signaling molecule that function downstream of SnRK2s, and it has been shown that PYL/PP2C-PYR/RCAR ABA receptor complex, the ABF-SnRK2/AREB pathway, play an important role as a regulator of ABAinduced stress signaling via ABRE-induced transcriptional activation of target genes associated on osmotic stress responses (Fig. 16.3) (Fujita et al., 2013; Yoshida et al., 2010, 2014; Vishwakarma et al., 2017). Transcriptome analysis has shown that almost two-thirds of downstream genes of subclass III SnRK2s are downregulated in the quadruple areb1/ areb2/abf3/abf1 mutant (Yoshida et al., 2014). These reports suggested that such SnRK2s control ABA-responsive transcriptional activation under osmotic stress mainly by the four AREB/ABF TFs (Yoshida et al., 2014, 2015). SnRK2.7/SRK2F and SnRK2.8/SRK2C are activated by ABA and participate in the drought-induced ABA-responsive transcript expression (Mizoguchi et al., 2010; Wang et al., 2018). Similar to AKS1 (ABA-responsive kinase substrate1), FBH3 (FLOWERING BHLH3) is downregulated in guard cells by OST1/SnRK2.6/SRK2E-dependent phosphorylation (Takahashi et al., 2013). FBH3/AKS1 transcriptionally activates KAT1 encoding K1 channel involved on stomatal opening (Fig. 16.3) (Takahashi et al., 2013; Yoshida et al., 2014). In addition, the ABA-stimulated OST1 protein kinase and SnRK2.3 were reported to directly interact and phosphorylate NADPH oxidases, which is in agreement with the reports that these NADPH oxidases are deployed in primary ABA-induced ROS signaling (Kwak et al., 2003; Danquah et al., 2014).

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independent signal transduction

405

ABF2/AREB1, ABF3, and ABF4/AREB2 are stimulated by drought, salt stress, and exogenous application of ABA to vegetative tissues, and the overexpressing of these factors demonstration increased tolerance of drought stress (Kim et al., 2004; Verma et al., 2016).

16.6 Abscisic acid
independent signal transduction Overall, ABA is known to be ubiquitous under osmotic stress, and this subsequently results in stomatal closure and prompts the transcriptional activation of numerous stressresponsive genes, for example, drought-induced expression of genes is controlled by pathways regulated independent of ABA (Yang et al., 2011; Joshi et al., 2016). Several signaling molecules have been reported, which are induced during abiotic stress in ABAindependent manner, and it has been indicated that CBF/DREB1 (CBF/DEHYDRATIONRESPONSIVE ELEMENT BINDING FACTOR) and DREB2 signaling molecules play a main role during stress (Fujita et al., 2013; Verma et al., 2013). The Arabidopsis genome contains eight DREB2 and six DREB1/CBF genes; among these genes, DREB2A/B get prompted during drought, salinity, heat and osmotic stress, and this matter shows the main part being played by CBF/DREB2 protein as a stress tolerance response (Fig. 16.3) (Nakashima et al., 2000; Verma et al., 2013). Under heat and osmotic stress conditions, overexpression of DREB2A plays critical roles in the expression of ABA-independent genes, which renders possibility to minimize the incompetent energy loss (Sakuma et al., 2002, 2006; Yoshida et al., 2014, 2015; Joshi et al., 2016). In Arabidopsis, it has been proposed that molecular regulators of cold stress signaling indicate DREB1/CBF family of TFs to confer cold tolerance, and overexpression of it increased abiotic stress tolerance (Huang et al., 2009). Since DREB2A prompts that numerous gene-encoding proteins convoluted in osmotic stress response (Kim et al., 2011a) have harmful impact on plant growth as indicated by expression at transcriptional and translational, and this matter is still under investigation. It has recently been recognized a novel transcriptional regulatory mechanism of DREB2A by growth-regulating factor 7 (GRF7), as a suppresser of osmotic stress
induced genes including DREB2A (Kim et al., 2011a, 2012; Yoshida et al., 2015). In comparison to wild type plants grown under control conditions, the transcript analyses have showed that stress-responsive genes of the osmotic stress
mediated pathway are activated in the grf7 mutant, indicating that GRF7 is a suppresser controlling the expression of a wide array of osmotic stress
inducible genes during control conditions (Kim et al., 2011a, 2012; Yoshida et al., 2015; Singh and Laxmi, 2015). On the other hand, except transcriptional repression under unstressed conditions, a ubiquitin
proteasome pathway is suggested to degrade leaky DREB2A expression, which is named DRIP1 (DREB2A-INTERACTING PROTEIN1), that overexpression of it delays the DREB2A expression downstream genes under dehydration stress (Qin et al., 2008; Yoshida et al., 2015). DRIP1 and DRIP2 are able to regulate negatively the expression of drought stress
inducible genes via targeting DREB2A to 26S proteasome-mediated proteolysis (Yoshida et al., 2015; Zhang et al., 2017).

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16.7 Auxin AUX is ubiquitously found, and multipurpose phytohormone and signaling molecule play crucial roles in most of the plant growth and developmental aspects (Jiang et al., 2017). This has encouraged investigation into physiological roles and molecular control of AUX in response to environmental stress. Recent findings indicate that environmental signals, for example, heavy metals, drought, and salinity prompt intonations of the biosynthesis of AUX, homeostasis, and the signal transduction pathways letting for effective cell responses under stress (Iglesias et al., 2010; Saini et al., 2017). In plants, the pool of AUX involves the mixture of free and conjugated AUX, the inactive precursor, and inactive methylated form of AUX (Normanly, 2010; Ludwig-Mu¨ller, 2011). AUX presence and concentration in plants is regulated by its biosynthesis, reversible and irreversible conjugation, degradation, accumulation, and transport processes (Sharma et al., 2013b, 2015a). The AUX concentration, AUX gradient, cell-to-cell transport, and celltype-dependent response together with its signaling pathway allow its contribution in almost developmental cues and growth directions in reaction with environmental stress (Salopek-Sondi et al., 2017; Saini et al., 2017). The major naturally forms of AUX in plants as free or conjugated forms consist of IAA (indole-3-acetic acid), IBA (indole-3-butyric acid), PAA (phenylacetic acid), 4-chloroindole-3-acetic acid (Ludwig-Mu¨ller, 2011).

16.8 Auxin biosynthesis AUX is known to be produced in the meristematic region of the primary shoot, roots, and young leaves and then transported through long distance to other parts of the plants (Jiang et al., 2017). AUX is mostly synthesized through Trp-independent and tryptophan (Trp)-dependent pathways (Mano and Nemoto, 2012). Trp has been proposed as a major precursor in the biosynthesis of IAA, and Trp-dependent pathway was introduced as the main route of AUX biosynthesized. In this pathway, different interconnected pathways have been contributed to IAA biosynthesis such as (1) the indole-3-acetamide pathway; (2) the IAOx (indole-3-acetaldoxime) pathway; (3) the IPA (indole-3-pyruvic acid) pathway; and (4) the TAM (tryptamine) pathways (a substrate proposed for the YUC flavin monooxygenases) (Fig. 16.4). These pathways are reviewed by Gao and Zhao (2014), Boot et al. (2016), and Jiang et al. (2017). The YUCCA flavin-containing monooxygenases, found as a key enzyme, catalyzes the rate-limiting step of Aux biosynthesis. The gene coding this enzyme is known as a key AUX biosynthesis gene from the activation tagging screen for the long hypocotyl Arabidopsis mutants (Zhao et al., 2001). The biosynthesized pool of IAA is modulated in plant cell by irreversible and reversible conjugations. IAA conjugation occurs in binding IAA to amino acids (amide-linked amino acid conjugate), peptide, and proteins, or sugars (ester linked). Therefore beside the de novo biosynthesized, the free IAA also can produce by releasing from conjugated form (storage pool) or from IBA (Mano and Nemoto, 2012; Wang and Estelle, 2014). These reversible and irreversible conjugations of AUX are very effective in the adjustment of the active hormone content throughout plant growth in different environmental stress

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16.9 Auxin signaling

FIGURE 16.4

A schematic representation of the IAA biosynthesis pathway. IAA, Indole-3-acetic acid.

YUC TAM

407

HTAM

TDC IAOx

Trp

IAM

TAA1

IAN

IPA YUC

IAA

(Gao and Zhao, 2014). The hydrolysis and release-free IAA pool from the conjugates can be more flexible and quicker than de novo biosynthesis. In addition, to de novo synthesis and conjugate release of IAA, the alteration of IBA to IAA by peroxisomal β-oxidation is another pathway, which lead to free IAA synthesis in plant cell (Zhao, 2010; Gao and Zhao, 2014). The availability and accumulation of active AUX in plant cell, which is essential for making AUX gradient and plant growth and development, is also regulated by AUX transport through different transport system (Zazimalova et al., 2010; Saini et al., 2017). AUX is transported by two different pathways (Zazimalova et al., 2010; Mano and Nemoto, 2012; Rosquete et al., 2012): phloem transport (nondirection and long-distance transport) and cell-to-cell transport (slower, directional, and short distance). Depending on the protonation of IAA, cell-to-cell transport consists of two distinct routes, such as passive diffusion (by plasma membrane) and active transport (by influx and efflux carriers), which is termed polar AUX transport (Balzan et al., 2014). The AUX polar transport provides more homeostasis in different environmental conditions and different hormone gradient. AUX biosynthesis, conjugation, and polar transport are affected by abiotic stress. It has been demonstrated that the level of active AUX and AUX responses in different plant species can be affected by different kinds of abiotic stress (Boot et al., 2016; Jiang et al., 2017).

16.9 Auxin signaling AUX signaling and cellular functions mediate by activating a family of TFs introduced as ARF (AUXIN RESPONSE FACTORS) (Fig. 16.5). Briefly, three proteins, namely, AFBs/ TIR1 (AUXIN SIGNALING F-BOX PROTEINS/TRANSPORT INHIBITOR RESPONSE 1), ABP1 (AUXIN BINDING PROTEIN1), and SKP2A (S-PHASE KINASE-ASSOCIATED PROTEIN 2A) is well-known as AUX receptors, each mediating AUX signal transduction

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U

Ask1

SCF

Cullin

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E2 U

AUX

Ask1

TRI1/AFB

TRI1/AFB

+AUX

Aux/IAA

U

U

U U

Proteasome 26S Aux/IAA ARF

ARF

The expression of AUX-response genes

FIGURE 16.5

A model of the AUX signaling pathway. AUX, Auxin.

cascades that in turn regulate plant growth under different environmental and intrinsic conditions (Salopek-Sondi et al., 2017; Saini et al., 2017; Jiang et al., 2017). TIR1 is a wellknown acceptable AUX receptor existing as a part of TIR1/AFB proteins, which are the subunits of SCFTIR1/AFB (Wang and Estelle, 2014; Korasick et al., 2013; Powers and Strader, 2016). Changes in AUX level are perceived by AUX receptors to initiate AUX signaling. Once AUX level is increased in the cell, TIR1/AFBs binds to the AUX, resulting ARF TFs activation and elicit AUX-mediated signaling cascade that causes the expression of AUX responsive genes (Fig. 16.5) (Korasick et al., 2013; Powers and Strader, 2016). AUX prompts transcriptional activation of three families of genes, namely, GH3, IAA/Aux, and the SAUR (small AUX-up RNA) (Woodward and Bartel, 2005; Sharma et al., 2013b). Under certain situations, where levels of AUX are either less or lost, the IAA/Aux protein repressors bind to the ARFs and then suppress their transcriptional activity (Fig. 16.5). The interaction between the ARF TFs and the IAA/Aux corepressors is a basic event of AUX signaling transduction (Fig. 16.5). In addition, ARFs bind directly to AuxREs (AUXresponse elements) in the promoter region of the AUX-inducible genes via DNA-binding domain (Korasick et al., 2013; Sharma et al., 2013b). Some evidence designated that AUX signaling is regulated under different abiotic stresses. For example, under drought stress, the TLD1/OsGH3.13, encoding IAA-amido synthase, increases the LEA genes expression that is associated with the improved drought stress tolerance in rice (Zhang et al., 2009a). AUX receptors, such as OsAFB2, OsTIR1, and OsCUL1, were also found to be regulated via drought, cold, and heat (Xia et al., 2012; Saini et al., 2017). It has been perceived that the transcriptional level of OsTIR1 was enhanced under stress, for example, drought and heat stress, whereas it is reduced under cold stress (Du et al., 2013). Furthermore, the gene expression of OsAFB2 was decreased under cold stress. These show that AUX signaling pathway may also be triggered by different abiotic stress, for instance, osmotic-like salinity repressed the TIR1 and AFB2 receptors (Chen et al., 2012a). The tir1/afb2 Arabidopsis mutant showed improved tolerance against osmotic stress in comparison to wild type (Iglesias et al., 2010; Salopek-Sondi et al., 2017).

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16.10 Brassinosteroids BRs are a class of polyhydroxylated steroidal plant hormones (analogous to animal steroid hormones in structure), which regulate growth and development of plant through creating a diverse array of biochemical and physiological modifications (Khripach et al., 2000; Clouse, 2011; Tang et al., 2016). In addition, BRs play vital roles in different plant growth
related processes, the division and elongation of cells, differentiation of vascular system and stomata, regulation of ROS metabolism, responses to gravitropism, biosynthesis of ET, improving plant responses to abiotic stress, and improving crop productivity against abiotic stress (Krishna, 2003; Bajguz and Hayat, 2009; Gudesblat and Russinova, 2011; Tang et al., 2016). The information obtained the genetic manipulation in the perception, biosynthesis, or conversion of BRs suggests a distinctive opportunity of meaningfully increasing the yield of crop plants (20%
60%) via both affecting the metabolic activities of plants and protecting the plants against abiotic stress (Divi and Krishna, 2009; Vriet et al., 2012; Zhang et al., 2014a; Marakli and Gozukirmizi, 2016; Tang et al., 2016; Liu et al., 2017). The studies on BR effects regarding plant stress responses together with BR signaling mutants, and genome-wide expression data can provide convincing evidence to introduce the roe of BR in enhancing plant tolerance against environmental stress (Divi and Krishna, 2010). Recent research proposes stress-impact justifying the roles of BRs in different plants influenced by various abiotic stresses such as high temperature, salinity, drought, metals/metalloids, and organic pollutants (Kagale et al., 2007; Bajguz, 2010; Ahammed et al., 2012, 2015; Zhang et al., 2014a; Sharma et al., 2015b, 2017; Wang et al., 2017). Recently, it has been considered that BRs are now to be potent ameliorants of heavy metal stresses (Vardhini, 2015; Rajewska et al., 2016).

16.11 Brassinosteroid biosynthesis Brassinolide (BL) is the active BR and up to now, .70 BL-related phytosteroids have been recognized from plants, and they are collectively called BRSs which are a group of polyhydroxylated steroidal hormones ubiquitously found in almost all plant species (Zhao and Li., 2012). Initially, during four hydroxylation steps, the campesterol is reduced to campestanol (Fig. 16.6). BL is synthesized from campesterol through two parallel paths including the early C-6 and late C-6 oxidation pathway (Noguchi et al., 2000; Clouse, 2011). At early C-6, campestanol is subsequently further hydroxylated to yield teasterone, which is followed by epimerization of the hydroxyl function, making typhasterol, with 6dehydroteasterone (as an intermediate) (Fig. 16.6). Typhasterol is more hydroxylated, ensuing in castasterone, which is finally transformed to BL (Noguchi et al., 2000). At late C-6, 6-deoxoteasterone is formed from campestanol, via subsequent hydroxylations (Noguchi et al., 2000; Chung and Choe, 2013). This phase is followed by an epimerization to yield 6-deoxotyphasterol, similar to the conversion from teasterone to typhasterol at the early oxidation paths (Fig. 16.6). Finally, 6-deoxotyphasterol is hydroxylated, creating castasterone (Fig. 16.6) (Clouse, 2011). The conversion of campestanol to 6-oxocampestanol to cathasterone (Early C-6 oxidation) and of 6-deoxocathasterone (Late C-6 oxidation) are

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FIGURE 16.6

A schematic representation of the BL (as active BR) biosynthesis pathway (Choudhary et al., 2012; Chung and Choe, 2013). BL, Brassinolide; BRs, brassinosteroids.

both done by DWF4, which is a rate-determining step in BL production (Chung and Choe, 2013). AUX stimulates BR biosynthesis through inhibiting the BZR1 binding to the DWF4 promoter (Chung et al., 2011; Chung and Choe, 2013).

16.12 Brassinosteroids signaling During BR signaling, a cell surface receptor family, which has leucine-rich repeat (LRR) receptor kinases BRI1 (BRASSINOSTEROID INSENSITIVE1) are responsible for the BR perceive (Wang et al., 2001b; Belkhadir and Jaillais, 2015; Martins et al., 2017; Nakamura et al., 2017). BRI1 is able to interact with BAK1 (BRI1 ASSOCIATED RECEPTOR KINASE1) as coreceptor, and this undergoes dephosphorylation and phosphorylation cascades to transfer information to the cell nucleus and regulate the expression of numerous genes, which are reported to be involved in various biochemical and physiological processes under (a)biotic stresses (Fig. 16.7) (Wang et al., 2001b; Sharma et al., 2013a, 2017; Belkhadir and Jaillais, 2015; Nakamura et al., 2017). The phosphorylation regulation process at the BRI1 receptor can involve in improving tolerance against abiotic stresses (Oh et al., 2012). For example, it has been suggested that BRI1 can integrate temperature and BR signaling to regulate growth during long-term changes in environmental conditions related with global warming (Martins et al., 2017). When there are no BLs, BRI1 act as an inactive homodimer due to the interaction between BKI1 and its cytoplasmic domain, inhibiting the hetero-dimerization of BAK1 with BRI1 (Fig. 16.7) (Choudhary et al., 2012). BAK1 belongs to the SERKs (somatic embryogenesis receptor kinases) subfamily (Choudhary et al., 2012). In Arabidopsis, this subfamily consists of five members, and BAK1 is as well as designated as SERK3, which are essential to the early processes of the BR-induced signaling pathway (Choudhary et al., 2012; Gou et al., 2012). In the presence of BRs, the signal is perceived through BRI1, Plant Life under Changing Environment

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FIGURE 16.7 An overview of the BR signaling pathway in the absence and in the presence of BR. BR, Brassinosteroid. Source: Modified from Choudhary, S.P., Yu, J.-Q., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.-S.P., 2012. Benefits of brassinosteroid crosstalk. Trends Plant Sci. 17, 594
605; Belkhadir, Y., Jaillais, Y., 2015. The molecular circuitry of brassinosteroid signaling. New Phytol. 206, 522
540.

LRR-RLKs, which interacts with its SERK3/BAK1 in BR-induced signaling (Choudhary et al., 2012). With binding of BR to the extracellular BRI1 domain promotes its kinase domain that phosphorylates BRI1—a downstream negative regulator (Fig. 16.7) (Wang et al., 2001b; Wang and Chory, 2006; Choudhary et al., 2012). It has been suggested the phosphorylated BKI1 is cleaved from the cell membrane, enabling BRI1 to deploy its BAK1 (an LRR RLK), distinct from BRI1 (Wang et al., 2001b; Nam and Li, 2002; Jaillais et al., 2011; Choudhary et al., 2012). Besides, detached BKI1 is able to increase BR signaling by antagonizing 14-3-3 proteins, which are intricated in the binding of BRASSINAZOLE RESISTANT 1 (BZR1) (as a principal regulator controlling BR-related expression of gene) and BES1 (BRI1-EMS SUPRESSOR1), as a TF responsible for BR-induced transcript expression, the two major TFs involved in BR signaling (Fig. 16.7) (Yin et al., 2002; Ryu et al., 2010; Jaillais et al., 2011; Choudhary et al., 2012). When BR signaling is activated, an activated BZR1 binds to the BR biosynthetic gene promoters and represses their expression, and in contrast, when cellular BR levels decline, BZR1 is transformed into an inactive form by phosphorylation via BIN2 (Fig. 16.7) (Chung and Choe, 2013). Activated BRI1 phosphorylates constitutive differential growth1 and BR signaling kinases (BSKs), which subsequently stimulate the protein phosphatase, BSI1 (BRI1 suppressor1), which in turn inactivates BIN2 via dephosphorylation, and then this dephosphorylation mitigates the suppression of BIN2 on BES1 and BZR1 (Tang et al., 2008; Clouse, 2011; Kim et al., 2011b). The accumulation of dephosphorylated BES1 and BZR1 is able move to nucleus in order to modulate the expression pattern of BR-related gene Plant Life under Changing Environment

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directly or through an association with other types of TFs (Li, 2010; Li et al., 2010; Choudhary et al., 2012). The other regulation mechanism of the BRI1-receptor kinase activity is BRI1 dephosphorylation via PP2A (protein phosphatase 2A), which causes BRI1 downregulation and the subsequently related signaling pathway (Fig. 16.7) (Di Rubbo et al., 2011; Gruszka, 2013). Also, during BR signaling, PP2A acts as a positive regulator by the dephosphorylation of BES1 and BZR1 TFs, which induces their accumulation and activation in the nucleus, and thus the BR-regulated expression of target genes (Fig. 16.7) (Nakamura et al., 2003; Ye et al., 2011; Gruszka, 2013). BR-induced genes deploy several molecular links to the specific subcellular processes, and also response to stress. Generally, the process of BR-mediated signaling is reported to positively modulate tolerance against (a)biotic stress both via BRs application and also through genetic deactivation of negative regulators on BR signaling (Nakamura et al., 2003; Koh et al., 2007; Divi et al., 2010; Sharma et al., 2013a). BRs indirectly or directly modulate various stressresponsive TFs via their negative regulators, such as BIN2 and BES1/BZR1 TFs, resulting into the triggering of stress-acclimation signal transduction pathways (Sharma et al., 2017). The expression of BR-inducible genes is regulated by BES1 and BZR1 also additional interacting TFs, and both BES1 and BZR1 interact with the PIF (phytochrome-interacting factor), which regulates a main transcription network, providing the coregulation of plant growth through BR and environment stress
related signals, and also the GA signaling DELLA proteins (Bai et al., 2012; Li et al., 2012a; Gallego-Bartolome´ et al., 2012; Oh et al., 2012; Zhu et al., 2013). The fundamental function on BR signaling is played via BIN2 as a major regulator (negative) of BR-induced signaling, which cause phosphorylation and consequently prevent TFs to regulate the transcriptional activation of targeted genes (Fig. 16.7) (Zhang et al., 2009b; Gruszka, 2013; Sharma et al., 2017). The Arabidopsis BIN2, regulating several physiological processes, responses to salinity stress (Gruszka, 2013). Exposure to salinity and drought stress enhances the expression of BSK5, which regulates stomatal closure process (ABA-dependent) during drought stress (Li et al., 2012b; Gruszka, 2013). The cell wall integrity activates BR signaling, which prompt the expression of numerous the extension of cell wall and loosening enzymes including pectin lyase-like, xyloglucan endotransglucosylase/hydrolase, and expansins to enhance cellular expansion (Uozu et al., 2000; Wolf et al., 2012; Rao and Dixon, 2017). Also, BRs signaling has been known to be essential for enhancing pectin methylesterases and leads to enhanced activity through changing the expression pattern of AtPME41, which is related to the stress responses and resistance mechanisms (Qu et al., 2011; Kim et al., 2012; Wolf et al., 2012). It has also been shown BRs are able to regulate MAPK and MAPK kinase kinase (MAPKKK) YDA (also known as YODA) to decrease the conductance of stomatal and this might help as one of the strategies for BRs prompted drought and salt (Sharma et al., 2017; Kim et al., 2012). Indeed, BR negatively regulates the development of stomatal through preventing BIN2 mediated phosphorylation and deactivation of YODA, which cause MAP kinase cascade activation (Kim et al., 2012). BR can also enhance NADPH oxidase activity and elevate H2O2 levels (Fig. 16.7), which are able to prompt the expression pattern of both of the regulatory genes, MAPK1 and MAPK3, and also the genes involved in antioxidant defense system (Sharma et al., 2017). Thus the BR-mediated stress tolerance is mostly linked with increased hydrogen peroxide (H2O2) accumulation that in turn activates MAPK cascade (Fig. 16.7), which prompts

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NADPH oxidase for self-propagation of H2O2 causing a positive increase in the signal loop (Xia et al., 2009; Jiang et al., 2012a,b; Sharma et al., 2017). This process has often been suggested in oxidative stress
induced via heavy metals stress, and BRs exogenous increase the tolerance to numerous stresses such as oxidative and heavy metals stresses (Vardhini and Anjum, 2015; Rajewska et al., 2016).

16.13 Ethylene ET is a gaseous phytohormone, which plays a crucial role in different plant developmental processes including flower and fruit ripening and senescence, pollination, germination, leaf and petal abscission, root formation, epinasty stimulation, and gravitropism, along with in plant responses to numerous stresses (Abeles et al., 1992; Wilmowicz et al., 2008; Gamalero and Glick, 2012; Upreti and Sharma, 2016). During metal stress conditions, plants display a rapid increase in ET production and reduced growth and development of plant, indicating a strong involvement of this phytohormone in plant response to heavy metal toxicity (Maksymiec, 2007; Schellingen et al., 2014; Bu¨cker-Neto et al., 2017). It has been suggested that, ET and ABA show a clear antagonism in regulating the stomatal movement, and both of them dynamically control the stomatal behavior and seem to be, ABA-induced stomata closure, which delayed by increased ET level (Tanaka et al., 2005).

16.14 Ethylene biosynthesis ET biosynthesis is performed from the precursor of methionine through S-adenosyl-Lmethionine (S-AdoMet), and ET synthesis is accomplished by three enzymes (1) S-AdoMet synthetase, which convert methionine to 1-aminocyclopropane-1-carboxylic acid (ACC); (2) ACC synthase, that hydrolyze S-AdoMet to ACC and 5-methylthioadenosine; and (3) ACC oxidase, which convert ACC to ET, CO2, and cyanide (Fig. 16.8) (Yang and Hoffman, 1984; Kende, 1989; Gamalero and Glick, 2012). ET biosynthesis is considerably controlled by internal signals throughout developmental phases and also in response to different stimuli from (a)biotic stresses (Wang et al., 2002).

16.15 Ethylene signaling The studies and investigates of the signaling of ET in physiological processes as well as stress responses can enhance our knowledge of how plants respond to endogenous signals and various environmental factors (Wang et al., 2013a). Generally, ET-responsive elementbinding factors (ERFs) influence a number of developmental processes and are also important for improved adaptability of plants under abiotic stresses such as heat and drought stress (Ecker, 1995; Nakano et al., 2006; Wani et al., 2016). The ET signal transduction pathways started with the ET perception by a five membrane-associated receptors, including ETR1/2 (ethylene resistant1/2), ETS1/2 (ethylene response sensor1/2), and EIN4 (ethylene insensitive 4), which negatively regulate ET responses (Chang and Stadler, 2001; Qiu et al., 2012).

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Met S-AdoMet synthetase S-AdoMet S-AdoMet ACC synthase ACC ACC oxidase Ethylene

FIGURE 16.8 A schematic representation of the ET biosynthesis pathway. ET, Ethylene. Source: Modified from Wang, K.L.-C., Li, H., Ecker, J.R., 2002. Ethylene biosynthesis and signaling networks. Plant Cell 14, S131
S151.

ETR1

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FIGURE 16.9

A model of the ET signaling pathway. ET, Ethylene.

With the association of ET to the receptors or in the absence of the receptors, constitutive triple response1 (CTR1) might not be triggered to phosphorylate EIN2 (Fig. 16.9) (Huang et al., 2003; Qiao et al., 2009; Qiu et al., 2012). In the absence of ET, receptor CTR1, that phosphorylates and subsequently results in the degradation of EIN2, thereby reduces

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ˇ ´ et al., 2016). EIN2 undergoes proteolytic cleavage the stability of ET TFs (Fig. 16.9) (Cerny through a proteasome to release an NLS (nuclear localization signal) that enters the nucleus to transduce information to the EIN3 and EIL1 (EIN3-LIKE1) TFs, which are the key TFs for ET early gene expression (Fig. 16.9) (Chang et al., 2013; Zhang et al., 2014b). Actually, by the activity of two F-box proteins (EBF) in E3 ubiquitin ligase complexes, EIN2 is degraded through 26S proteasome activity EIN2-targeting F-box protein1/2 (Qiao et al., 2009; Cho and Yoo, 2015). Also, in the absence of ET, EIN3 is a continuousdegradation process (Fig. 16.9), which is regulated by these two F-box proteins, EBF1/2 (EIN3-binding F-box protein1/2) (Potuschak et al., 2003; Guo and Ecker, 2003; Gagne et al., 2004; Qiao et al., 2009; Cho and Yoo, 2015). The serine/threonine kinase activity of CTR1 is able phosphorylate EIN2 (Fig. 16.9), which prevents the movement of the C-terminal domain of EIN2 into the nucleus and accordingly prevents ET signaling (Huang et al., 2003; Ju et al., 2012; Zhang et al., 2014b). The similarity of CTR1 with Raf, a mitogen-activated protein kinase3 (MAPKKK), is very high in sequence (Kieber et al., 1993); it was reported to play a role, like Raf, in a classic MAPK cascade (Fig. 16.9). However, the MAPKKs/MAPKs which is regulated by CTR1 was not approved, and some reports for the existence of these kinases in ET signaling are controversial (Ju and Chang, 2012; Hahn and Harter, 2009; Cho and Yoo, 2015). However, during abiotic stress, MAPKs are involved in the ET signaling, and it has been shown that MPK3 and MPK6 play a critical role in the control of ET response pathway by promoting the stabilization of EIN3 (Hahn and Harter, 2009). Besides, MAPKs (MPK3 and MPK6) can phosphorylate ACS that leads to an enhanced ET production and activation of ET signaling (Fig. 16.9). On the other hand, when there is ET, a part of EIN2 accumulates in the nucleus of plant cell that associates well with the accumulation of EIL1 and EIN3 in the nucleus (Fig. 16.9) (Qiao et al., 2012; Ju et al., 2012; Wang et al., 2013a). The amassing of EIL1 and EIN3 in the nucleus induces transcription initiation via EIN3-binding in the promoter region of targeted genes such as EBF2 and ERF1 (Fig. 16.9), which act as a transcriptional activator by recognizing specifically the GCC elements in the promoter region of ETresponsive secondary genes (Solano et al., 1998; Konishi and Yanagisawa, 2008). Finally the products of genes related to these transcription cascades cause change in the cellular and biochemical process, made different plant growth and developmental process adaptive in response to ET (Solano et al., 1998; Konishi and Yanagisawa, 2008; Cho and Yoo, 2015). In addition, EIN3 can directly target multiple downstream targets which are responding to different stress factors (Zhang et al., 2011; Zhu et al., 2011; Wang et al., 2013a). EIN3, as a nuclear-localized protein, is a positive regulator of ET signaling and mutants in EIN3 display reduced sensitivity to ET (Wang et al., 2013a). It has been indicated that EIN3 is able to target directly the ESE1 promoter region (ethylene/salt-induced ERF1), a key modulator of the ESE1 expression and salinity response, and enhance ectopically expressing EIN3 (Zhang et al., 2011; Wang et al., 2013a). The expression of ERF gene can be prompted via ET and salt, that way with binding ESE1 to DRE and GCC box, that are localized in the promoter region of salt stress
induced genes (COR15A, HLS1, P5CS2, and RD29A) (Zhang et al., 2011; Wang et al., 2013a). The overexpressing EIN3 or ESE1 controls the expression pattern of salt stress
induced genes, which leads to increasing their stress tolerance (Wang et al., 2013a). Interestingly, EIN3 is a direct target of signal response 1, which is ET-responsive gene NtER1 that play an important role in some stress

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responses such as wounding, temperature, salinity, ET, and ABA (Yang and Poovaiah, 2002). During heavy metal stress, it has also been observed as an increasing expression of the EIN3 gene (Trinh et al., 2014; Keunen et al., 2016). Furthermore, it has been found that some of the jasmonate ZIM-domain (JAZ) proteins as transcriptional repressors interact with EIN3 (Wang et al., 2013a; Zhu et al., 2011). The EIL1/EIN3 function could be suppressed via JAZs, which recruit histone deacetylases 6 to bind EIL1/EIN3 forming a complex that represses the DNA-binding of EIN3 and prevent JA-induced signaling (Wang et al., 2013a). Thus EIL1/EIN3 serves as a node to link ET and JA signaling and control the plant adaptive response mechanisms to various stressors (Wang et al., 2013a). In addition, there is a link between the CTR1/EIN3-dependent ET and GA DELLA signaling pathways that assist adaptive regulation of plant’s life cycle progress in reaction to environmental difficulties (Achard et al., 2007). ET is reported to mediate a various range of signal transduction process during heavy metal stress, and there are many reports that demonstrate improved ET production in plants exposed to metals, but the effects of metal stress on ET signaling regulatory mechanisms are not discussed obviously (Keunen et al., 2016). However, some reports support the role of ET signal transduction in stress responses, mainly related to ERFs proteins, which belong to AP2/ERF (Herbette et al., 2006; Dietz et al., 2010; Zhou et al., 2013b; Chen et al., 2014; Montero-Palmero et al., 2014; Dey and Corina Vlot, 2015). In overall, the molecular and genetic studies established the significant ERFs functions in response to abiotic stressors and occasionally impart multiple stress adaptabilities (Zhang et al., 2005; Wang et al., 2013a; Zhu et al., 2014; Dey and Corina Vlot, 2015).

16.16 Gibberellins GAs are acting as hormone and a great group of diterpenoid carboxylic acids (over 130 categorized GAs). However, a few classes of GA forms including GA1, GA3, and GA4 act as bioactive molecules in plants (Hedden and Thomas, 2012; Zawaski and Busov, 2014). The GAs are involved in regulating some growth and developmental processes, consisting of leaf expansion, germination of seeds, trichome initiation, stem elongation, pollen maturation, and the induction of flower and fruit development (Achard and Genschik, 2009; Yamaguchi, 2008; Davie`re and Achard, 2013). The results of several studies demonstrate that GAs, as classical hormones, are major targets for stress-induced growth-related processes (Magome et al., 2008). Adaptation to abiotic stress by GAs is mostly performed through DELLA proteins (Achard et al., 2006; 2008a; Magome et al., 2008). DELLA domain-containing proteins are potent suppressors of numerous GA-mediated responses that arbitrate the sensitivity of the protein to the proteolytic degradation process (Gallego-Bartolome´ et al., 2011). The role of GA on adaptation to abiotic stress was discussed and the response of Arabidopsis seedlings was subjected to osmotic stress (Skirycz et al., 2010; Claeys et al., 2012). Salt stress reduces the active endogenous GAs A. thaliana that corresponded with accumulation of DELLA (Achard et al., 2006).

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16.17 Gibberellin biosynthesis GAs are biosynthesized from IPP (Fig. 16.10). From IPP, 20-C geranylgeranyl diphosphate (GGDP) precursors of terpenoids are formed by condensation of 5-C units IPP. Later, GGPP is converted by two cyclization reactions through copalyI pyrophosphate into ent-kaurene, which is transported from plastids to ER membrane (Fig. 16.10). Then ent-kaurene is oxidized at several steps to form GA12-aldehyde, which is subsequently oxidized to give GA12 that is the precursor to all other GAs in plants (Fig. 16.10). Thus GGDP is a precursor of GAs via methylerythritol phosphate pathway (Ogawa et al., 2003). This metabolite was made in plastid through the two terpene cyclases localized in plastids, followed by oxidization in the ER through cytochrome P450 monooxygenases and subsequently by the soluble 2-oxoglutarate-dependent dioxygenases (Yamaguchi, 2008; Hedden and Thomas, 2012). This dioxygenase complex involves GA 3-oxidase (GA3ox), GA 20oxidase (GA20ox), and isozymes (Kaneko et al., 2003; Sharan et al., 2017). Several studies revealed the important effects of dioxygenase-encoding genes as the crucial regulating sites of GA biosynthetic pathway due to environmental and developmental signals, especially GA2ox transcripts, that are responsible for abiotic stressors (Magome et al., 2008; O’Neill et al., 2010; Shan et al., 2014). The expression pattern of some paralogues within

IPP

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FIGURE 16.10

GAn

A schematic representation of the GA biosynthesis pathway. GA, Gibberellin.

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the GA2ox, GA3ox, and GA20ox gene families is controlled via GA action, the downregulation of biosynthesis genes, while the expression of GA2ox transcript is upregulated, thus providing GA-mediated homeostasis (Weston et al., 2008; O’Neill et al., 2010).

16.18 Gibberellin signaling The essential constituents of the GA signal transduction pathways are including the DELLAs (DELLA growth inhibitors) and the F-box SLY1 proteins (SLEEPY1), and GID1/2 (GA receptor gibberellin insensitive dwarf1/2) (Achard and Genschik, 2009; Colebrook et al., 2014) (Fig. 16.11). In the GA action mode, DELLA imprisons the growth of plant, while the GA-induced signal stimulates the growth through minimizing DELLAdependent growth restriction (Achard and Genschik, 2009; Sharan et al., 2017). The GA signal is perceived by GID1 (Fig. 16.11), which contains two features including GAbinding pocket (the hormone-sensitive lipase catalytic domain) and a flexible N-terminal extension (Murase et al., 2008). Although the main location of this protein was reported nucleus but it seems to be localize in cytoplasm as well (Ueguchi-Tanaka and Matsuoka, 2010; Willige et al., 2011). The group “C3-hydroxyl” of the GA molecule converts H-bound to the Tyr31-residue of the GID1 by binding of bioactive GA. This reaction mediates a conformational alteration in the N-terminal part to cover the GA pockets (Murase et al., 2008; Ueguchi-Tanaka and Matsuoka, 2010). When the pocket is shut, the upper DELLA binds with the top surface of the lid to produce the GA-GID1 and DELLA complex, which makes conformational change in GRAS-domain of the DELLA that improve association between the LHRII and VHIID domains of F-box SLY1/GID2 and DELLA proteins (Griffiths et al., 2006; Ueguchi-Tanaka and Matsuoka, 2010; Willige et al., 2011; Hirano et al., 2012; Colebrook et al., 2014; Sharan et al., 2017). F-box proteins are a component of GA GID1

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FIGURE 16.11

A model of the GA signaling pathway. GA, Gibberellin.

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the SCF E3 ubiquitin ligase complexes that catalyze the degradation of polyubiquitin through the 26S proteasome (Fig. 16.11) (De Lucas et al., 2008; Dill et al., 2004). Therefore GA induces growth via mediating the proteasome-dependent destabilization of DELLA. DELLAs mediate their functions through interaction with different regulatory proteins classes such as PIFs (Weston et al., 2008; Ubeda-Toma´s et al., 2008; Gallego-Bartolome´ et al., 2010; Ni et al., 2013) and BZR1 (brassinazole resistant1) (Gallego-Bartolome´ et al., 2010; Bai et al., 2012; Gallego-Bartolome´ et al., 2012; Ni et al., 2013). Furthermore, DELLAs can bind to several transcription regulators (Gallego-Bartolome´ et al., 2010; Feurtado et al., 2011; Cheminant et al., 2011; Hong et al., 2012; Davie`re and Achard, 2013). Following these interactions, DELLAs are able to prevent the DNA-binding capability of TFs, for example, PIFs (Feng et al., 2008; de Lucas et al., 2008; Ni et al., 2013) or prevent the transcriptional modulator activity, for example, with JAZs (Hou et al., 2010; Ni et al., 2013); however, GA relieves DELLAs suppression through promoting their degradation via the 26S proteasome (Fig. 16.11). The authors proposed that different abiotic stresses constrain growth through the enhancement and decrease of GA and DELLA levels, respectively. Therefore plants alter the levels of DELLA and GA to improve the existence in critical conditions. This DELLAinduced growth inhibition, under abiotic stresses, can be mediated through enhancing the expression pattern of cell cycle inhibition proteins, and this pathway has beneficial effects for plants and adapts them in their fight for survival (Hauvermale et al., 2012; Colebrook et al., 2014; Sharan et al., 2017). DELLA promotes growth restrain by Kip-related protein 2 and Siamese (Achard et al., 2009). Results of other studies showed that different environmental changes could affect GAs signaling via alterations in GA2ox, GA3ox, and GA20ox expressions (Qin et al., 2011a; Hauvermale et al., 2012; Sun et al., 2013; Yang et al., 2014; Colebrook et al., 2014; Sharan et al., 2017). Spindyl (SPY) is known as stress-related genes, and negative regulator of GA signaling is induced due to abiotic stressors especially drought conditions (Qin et al., 2011a). This gene encodes an O-linked N-acetyl-glucosamine-transferase, and its mutation leads to plants high drought and salt tolerance (Qin et al., 2011a). Therefore it can be concluded that SPY has negative role in plants adaptation to abiotic stress. It is proposed that SPY changes DELLA protein activity or stability through O-GlcNac modification, then DELLA accumulation is attained by the dysfunction of SPY protein or spy mutants (Qin et al., 2011a). In A. thaliana, DELLA mediated the regulation of transcription that is associated with the control of the oxidative defense system against abiotic stress (Achard et al., 2008b). It was suggested that ROS accumulation under abiotic stress was restricted through DELLA activity, then ROS-activated plant damage can be also postponed by DELLA (Achard et al., 2008b; Sharan et al., 2017). Similarly, in rice, there is a link between optimized Slender1 (SLR1) levels, and decreased oxidative damage was studied in Sub1A lines affected by dehydration following flooding and to drought (Fukao et al., 2011). Furthermore, ROS seem to be active in regulating GA-mediated root growth that shows DELLA roles in plant growth and stress tolerance (Achard et al., 2008b). However, there is less knowledge of the relationship between GA signaling and GA role in the regulation of ROS level yet. During abiotic stresses, it has also been revealed that DELLA proteins regulate cross talk between GA and other phytohormones.

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16.19 Cytokinin CK regulates a varied range of critical processes related to plant growth (Werner and Schmu¨lling, 2009; Peleg et al., 2011; Kieber and Schaller, 2014; Zwack and Rashotte, 2015). It is known as the important inducer of cell division and the preservation of stem cells in shoots and roots apical meristems as well as is known as a crucial cell cycle regulator of plants (Gordon et al., 2009; Schaller et al., 2014; Zwack and Rashotte, 2015). CK has wellknown and functional roles in plants life at cell, tissue, and organ levels such as cell division and expansion (Chiang et al., 2012; Efroni et al., 2013), chloroplast biogenesis (Zubo et al., 2008), promotion of photosynthesis (Zubo et al., 2008), enhancement of sink strength (Peleg et al., 2011), differentiation of expanding leaves (Efroni et al., 2013; Zwack and Rashotte, 2015), leaves senescence inhibition, roots xylem and phloem differentiation (Ma¨ho¨nen et al., 2000; Bishopp et al., 2011; Thu et al., 2017), and development of vegetative and reproductive organs (Gordon et al., 2009). These multifunctional roles of CKs propose that changes in CK content under different environmental conditions such as stress or stimuli factors must play effective role in the course of plants’ adaptation to adverse factors. However, the interactions between CK and environmental stress or stimuli were not well understood (Argueso et al., 2009; Ha et al., 2012; Efroni et al., 2013; O’Brien and Benkova´, 2013; Thu et al., 2017). Numerous studies considered the negative CKs role in plants adaptation to various stressors (Zwack and Rashotte, 2015; Thu et al., 2017); this proposes that reduced level of CK is necessary for the improvement of plant resistance to abiotic stress. However, some evidences support both positive and negative responses of CK to abiotic stress. Experimental studies about CKs levels during stress response showed the temporary increase of hormone level upon exposure to stress, followed via reduction under sustained moderate stress when affected with more severe conditions (Veselov et al., 2017). The application of exogenous CKs was reported to affect the tolerance of plants to stress. Wheat seedling treated with CK and bean plants pretreated with CK revealed improved salt tolerance (Pospisilova and Batkova, 2004). Study of the effect of heat stress has shown to increase in the CK levels at the beginning of stress, whereas the hormone content was reduced when the duration of exposure was prolonged (Liu and Huang, 2002; Dobra et al., 2015). The deficiency in mineral nutrients after 24 hours decreased CK level in roots and shoots of studied plants through the activation of CK oxidase (Brugiere et al., 2003; Vysotskaya et al., 2009). Overall, the results of these studies designate different environmental stresses that affect the CK content, metabolism, and signaling, which can be varied based on spatial, temporal, and developmental context.

16.20 Cytokinins biosynthesis The CK level in plant cell determined by the balance between the rates of import and export, de novo synthesis, conversion of different forms, inactivates through glucosylation and catabolic reactions (Sakakibara, 2006; Fre´bort et al., 2011). The first proposed pathway was tRNA degradation that is the main source of active CKs (Fre´bort et al., 2011).

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IPP

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DMAPP

AMP

iPRMP

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FIGURE 16.12 A schematic representation of the tZ biosynthesis pathway (as the main pathway for CK synthesis). CK, Cytokinin; tZ, trans-zeatin.

CYP735A

tZRMP LOG

tZ

However, the determination of tRNA turnover degrees exhibited that a de novo biosynthetic pathway that differs from tRNA degradation must also be existing in plants (Yevdakova et al., 2008). CK de novo biosynthesis can be active to produce the inactive forms of nucleotides with phosphate (iP) (Sakakibara, 2010; Fre´bort et al., 2011). trans-Zeatin (tZ) biosynthetic pathway is the main step for CK biosynthesis in most of the plant species (Fig. 16.12). The synthesis of tZ can happen either directly by iP 50 -monophosphate riboside (iPRMP)-independent (iP) or indirectly by conversion from the precursor of iPRMP-dependent (iP) immediate (Sakakibara, 2010). The presence of an extra iPRMP-independent biosynthesis of the tZ has been confirmed, where the phytohormone is synthesized by IPT (adenylate-isopentenyl-transferase) utilizing a hydroxylated terpenoid side-chain donor (Sakakibara, 2010). Dimethylallyl diphosphate (DMAPP) is the main substrate for CK biosynthesis and is produced via isomerization of IPP (isopentenyl diphosphate) by the catalysis of isopentenyl diphosphate isomerase (Sakakibara, 2006) (Fig. 16.12). Later, IPTs catalyze the reaction between AMP and DMAPP to form iP iPRMP, which are subsequently converted to tZRMP (tZ-nucleotides) by CYP735A (CK trans-hydroxylase), and then tZRMP is subsequently converted to tZ by LONELY GUY; tRNA-IPT, tRNA-isopentenyltransferase (LOG) (Fig. 16.12). IPT enzyme catalyzes the rate-limiting step in CK synthesis, and in Arabidopsis, the AtIPT (A. thaliana IPT) involved nine members of genes, which elaborate the synthesis of tRNA-IPTs and ADP/ATP (Miyawaki et al., 2006; Thu et al., 2017).

16.21 Cytokinin signaling The CK defined as effective signal molecule in tiny concentration (1
50 pmol/g of FW; Galuszka et al., 2007). Its signaling activity can be done in meristemic tissues as a paracrine local signal and in plants’ nutrition availability (distal signals) (Sakakibara, 2006; Werner et al., 2010; Thu et al., 2017). CK signaling is a multistep-phosphorelay pathway (reviewed by Zwack and Rashotte, 2015; Thu et al., 2017) including HK (histidin kinase) protein family promoting as receptors, the histidine-containing phosphotransfer (HP) protein family acting as messengers, and response regulator (RR) protein family mediating the expression profile of target genes (Fig. 16.13). AHK1, AHK2, AHK3, AHK4, and CRE1 are the main HK receptors in plants (Tran et al., 2007, 2010; El-Showk et al., 2013).

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FIGURE 16.13

16. Phytohormonal signaling under abiotic stress

A model of the CK signaling pathway. CK, Cytokinin.

As illustrated in Fig. 16.13, the CK signal transduction in plants occurs as below. An HK perceive a CK signal, resulting in a histidine residue to become phosphorylated. Then this phosphate will be relayed to an asparagine residue and subsequently further to an Arabidopsis HP factor, which in turn will diffuse via the nuclear membrane and transfer the phosphate group to RRs that finally affect the transcription of DNA by a CK target gene (Fig. 16.13). RRs have been classified as type-A (ARRs) and type-B RRs (BRRS). ARRs are promptly induced in response to exogenous CKs (Shi et al., 2012). On the other side, the BRRs have been indicated to be the TFs that positively mediate C responses (Sakai et al., 2001). Therefore phosphorylation of triggers the GARP-motif-containing MYB-like TFs, which controls the expression of CK-responsive genes (Gupta and Rashotte, 2012). ARRs types are similar to BRRs but absent in DNA-binding GARP-motif, and it has also been suggested that these proteins compete with BRRs phosphorylation and negatively inhibit CK signaling (Gupta and Rashotte, 2012). Overall, the role of CKs in plant responses to abiotic stressors assisted largely through their role in cell division promotion, regulation of nutrients uptake, upkeep the identity of meristematic cell, and preservation of the redox potentials of meristematic cells under drought stress (Rivero et al., 2007; Werner et al., 2010; Gupta and Rashotte, 2012). The clarification of CK signaling pathway and components, particularly in Arabidopsis has enabled researchers to study the effects of this pathway against abiotic stress by using techniques such as reverse genetic approaches. CKs and CKs signaling components are known to have main roles in different abiotic stresses. However, the most variation range in CK signaling pathway in plant stress responses made it difficult to find out each component roles (Hwang et al., 2012; Zalaba´k

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et al., 2013). It has been found that the expression of CK-receptor-encoding genes is strongly affected via osmotic stress (Argueso et al., 2009). In this regard, Arabidopsis possesses four HKs (AHK1, AHK2, AHK3, and AHK4) that can act as stress sensors, which would transduce the CK-dependent signaling cascades (Urao et al., 2000; Jeon et al., 2010). For instance, AHK1 acts as a sensor of osmolarity, which positively regulate the drought stress tolerance and transfer the osmotic cross talk with a downstream CK-dependent signal transduction pathway (Urao et al., 2000; Tran et al., 2007; Kumar et al., 2013). By contrast, other CK receptors such as AHK2/3/4 are the negative regulators of the stress responses. In Arabidopsis, AHK2/3 activated by osmotic stress proposes the importance of CK sensitivity under this condition. Thu et al. (2017) studied the negative regulatory roles of AHK2 and 3 through drought stress tolerance assay of wild type plants and their single and double mutants. The expression of AHK3 was also reported in plants affected by cold and salinity stress (Tran et al., 2007). In CK signaling pathway, more than the CK receptors, the expression of downstream components (HPs and RRs) was affected under osmotic stress. The expression of HPs in Arabidopsis (AHPs) is inhibited by osmotic stress such as drought. Triple mutant plants (ahp2, ahp3, and ahp5) exhibit tolerance to dehydration stress (Nishiyama et al., 2013). Type-A of all ARRs are the important components of CK signaling pathway, which regulate their expression by abiotic stress. For instance, the type-ARR22 of Arabidopsis is upregulated in response to drought stress (Kang et al., 2012), and salinity increases the ARR5 transcript expression (Mason et al., 2010) in addition to ARR5, 6, 7, and 15 are upregulated by cold stress (Jeon and Kim, 2013; Jeon et al., 2010). Similarly, ARR5 upregulation depends on ARR1 and ARR12 in response to salinity (Mason et al., 2010). Moreover, typeBARR1 and ARR12 regulate sodium uptake in Arabidopsis shoots through mediating the expression pattern of AtHKT1;1 (Arabidopsis high-affinity K1 transporter 1;1) in roots (Mason et al., 2010). Three ARRs (ARR5, ARR7, and ARR15) are over expressed in Arabidopsis under freezing stress, which lead to its adaptation to this stress (Shi et al., 2012). The results of qRT-PCR analyses showed that the expression pattern of several CK signaling pathway genes in Arabidopsis against abiotic stress were reported to be diverse depending on the plant species, tissue or organ type, and the stress duration (Nishiyama et al., 2011, 2013; Zwack and Rashotte, 2015). These findings suggest that in response to stressors, the role played through CK-mediated signaling is more complex.

16.22 Jasmonic acid and salicylic acid JA as an oxylipin hormone is critical for optimal plant growth and variety of developmental responses, for example, germination, root elongation, pollination, fruit ripening, and plant senescence, as well as acting as stress modulator (Creelman and Mullet, 1997; Agrawal et al., 2003; Liu et al., 2016). It has also been documented that JA involves on crop response to (a)biotic stressors, for example, heat stress, drought, and salt and metal toxicity (Maksymiec et al., 2005; Clarke et al., 2009; De Ollas et al., 2015; Per et al., 2018). SA is an important phytohormone involved in the complex but well-coordinated stress signaling pathways in plants, for example, after exposure to salinity, osmotic, drought, and heat stress. Moreover, SA accumulation increases the activity of SA assimilation

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pathway enzymes such as serine acetyltransferase, glutathione (GSH), and finally enhanced metals resistance (Khan et al., 2015). In plants, Fe-deficiency induced chlorosis is also described to be reduced by the accumulation of SA (Kong et al., 2014). Furthermore, several key physiological processes, such as germination and seedling, were establishment; N metabolism, photosynthesis, cellular proliferation, stomatal aperture, respiration, antioxidant defense, and plant senescence are regulated by the presence of SA, thus improving abiotic stress tolerance capacity of plants (Hayat et al., 2010; Khan and Khan, 2013; Khan et al., 2015; Nazar et al., 2015). Interestingly, there is an interaction between JA and SA at various levels, for example, biosynthesis and stress signaling pathways, and it has been suggested that JA and SA are tightly linked biochemically and can be induced by multiple (a)biotic stresses, thereby leading to defense responses mainly by the activation of MAPK4 that acts as an activator of JA-mediated signaling and repressor of SA-mediated signaling (Brodersen et al., 2006; Khan et al., 2012b). Thus both these hormones represent an efficient target point for modulating plant metabolic activities under abiotic stresses (Khan et al., 2012b,c).

16.23 Jasmonic acid biosynthesis JAs are ubiquitously present in plant kingdom and represent cyclopentanone phytohormones that are derived from the membrane fatty acids metabolism particularly JA and MeJA (its methyl ester)—first identified in the essential oil of jasmine (Wani et al., 2016). The galactolipids of chloroplast membrane release α-linolenic acid (α-LeA; 18:3) that act as a fatty acid substrate for JA biosynthesis. The release of JA biosynthesis substrate, that is, α-LeA from the galactolipids at sn1 position is catalyzed by the enzyme phospholipase1 (PLA1) (Scherer et al., 2010). Previously, JA generation was thought to be dependent on defective in anther dehiscence1 (DAD1), due to decreased JA levels in flowers of dad1 mutant (Ishiguro et al., 2001). However, the subsequent identification of DAD1 as a target of homeotic-protein “AGAMOUS” strongly substantiated this function of DAD1 (Ito et al., 2007). The AGAMOUS protein was reported to bind to the DAD1 genomic region and play multiple roles in late stamen development such as dehiscence of anthers, maturation of pollen, and elongation of filaments (Ito et al., 2007). But this particular role of DAD1 remained doubtful involving the active role of PLA1s in JA biosynthesis in response to wounding. For instance, a PLA1 member of the Arabidopsis family, that is, DONGLE (DGL), was considered to be involved in JA biosynthesis under wounding stress (Yang et al., 2007). However, the data published by different research groups working with DGL and DAD1 lines remained contradictory. Nevertheless, the recently generated DGL and DAD1 RNAi lines were unresponsive to early wounding. The authors found that DGL protein was not localized in plastids as required for JA biosynthesis, but in lipid bodies, indicating their no involvement in JA biosynthesis (Ellinger et al., 2010). Furthermore, the authors screened 16 lipase mutants and found that only one mutant (PLA1y1; At1g06800) showed decreased JA level in wounded leaves (Ellinger et al., 2010). Besides, by the use of RNAi lines of GALACTOLIPASE A1 (GLA1), these Arabidopsis data were complemented and suggested its role in JA biosynthesis in roots and leaves of Nicotiana attenuata (Bonaventure et al., 2011).

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Generally, in chloroplast membranes JA biosynthesis is initiated by the oxygenation of α-LeA, where lipoxygenase (LOX) mediate the insertion of oxygen at the C atom 13 to form 13-13-HPOT (hydroperoxy-9,11,15-octadecatrienoic acid), that is subsequently converted to OPDA (cis-12-oxo-phytodienoic acid) by cyclic reaction via allene oxide synthase (AOS) (Fig. 16.14) (Wasternack and Hause, 2013). Then, OPDA has transferred ATPbinding cassette (ABC) transporter COMATOSE (CTS) to peroxisome, where OPDA is reduced to 12-oxophytoenoic acid by OPDA reductase, and then three β-oxidation cycles are occurred (Fig. 16.14) (Theodoulou et al., 2005; Wasternack and Hause, 2013). Thus OPDA act as precursor of LOX-catalyzed JA biosynthesis, which is extensively investigated in dicots including Arabidopsis, tomato, and tobacco (Yan et al., 2012). Among them, the Arabidopsis genome is characterized by the presence of six LOX members, and four out of which are 13-LOX-type (LOX2
LOX6); however, their exact role is not completely understood yet (Bannenberg et al., 2009). Among them, LOX2 was primarily reported to participate in early wounding response in plants that was later experimentally proved showing elevated JA biosynthesis within an hour of wounding (Schommer et al., 2008; Bell et al., 1995; Glauser et al., 2009). Later reports also showed the involvement of LOX2 in oxylipins formation in response to sorbitol stress and also dark stress
induced senescence (Seltmann et al., 2010). The complementary data using LOX2-RNAi lines found basal JA and OPDA levels but did not show bulk formation of JA during dark-induced senescence. The OPDA synthesized JA can be subsequently converted into numerous conjugates or intermediates, some of which have well-described biological activity such as JA, MeJA, cisjasmone, and JA-Ile (Yan et al., 2012).

Chloroplast

FIGURE 16.14 A schematic representation of the JA biosynthesis pathway. JA, Jasmonic acid.

α-LeA LOX

13-HPOT AOS

OPDA

CTS

Peroxisome OPDA OPDAR

OPC β-Oxidation JA JA

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FIGURE 16.15 A schematic representation of the SA biosynthesis pathway. SA, Salicylic acid.

ICS

Shikimicacid pathway

Chorismate

IC

IPL

Phe PAL

CA CinnamoylCoA

Coumaric acid

SA BAH2

Benzoyl-CoA

Benzaldehyde

BA

16.24 Salicylic acid biosynthesis In plants, SA, as a phenolic compound, is biosynthesized by two distinctive pathways that need chorismate as a major metabolite (Vlot et al., 2009). During cytoplasm-localized PAL (phenylalanine ammonia lyase) pathway, PAL is the primary enzyme and an important regulator in the phenylpropanoid pathway that chorismate-derived phenylalanine (Phe) is transformed into SA by either coumaric acid or benzoate intermediates and is activated under multiple (a)biotic stresses (Zhao et al., 2017). Cinnamic acid (CA) is synthesized from Phe by the PAL activity (Fig. 16.15). SA may be produced from CA by benzoic acid (BA) and/or ortho-coumaric acid that largely depends on the plant species, then CA is oxidized to BA by three potential biosynthetic pathways in plants, containing a cinnamoyl CoA β-oxidative pathway, a nonoxidative pathway from cinnamoyl CoA, and a nonoxidation pathway from CA to BA (Fig. 16.15) (Horva´th et al., 2007; Zhao et al., 2017). Subsequently, SA is produced by the BA hydroxylation catalyzed by BA2H (benzoic-acid-2 hydroxylase) (Fig. 16.15) (Zhao et al., 2017). It has been suggested that water shortage affected the PAL activity and BA2H, which were convoluted in biosynthesis of SA from Phe (Bandurska et al., 2012). In addition, SA is also biosynthesized from by chorismic and iso-chorismic acid that was initially reported in bacteria; subsequently, it was also reported to occur in plant chloroplasts (Wildermuth et al., 2001). Chorismate is converted into SA through isochorismate (IC) in biphasic pathway catalyzed by the IC pyruvate lyase and IC synthase (Fig. 16.15) (Wildermuth et al., 2001; Horva´th et al., 2007). Interestingly, the major enzymes of SA biosynthetic pathways are reported to be modulated by multiple abiotic stresses, thus leading to enhanced SA production under such conditions and ultimately increase the tolerance of plants against stress (Horva´th et al., 2007).

16.25 Jasmonic acid signaling JA is a key signaling phytohormone that regulates multiple plant responses to environmental stresses (Tuteja et al., 2010). JA acts as a stress signal with other intermediates of

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JA coregulatory pathways. JA signaling can be induced by diverse biotic stresses, for example, pathogen attack, abiotic stressors, for example, wounding, salinity, drought, osmotic stress, low temperature, and exposure, to multiple elicitors such as oligosaccharides, oligogalacturonides, chitin, and yeast extracts (Turner et al., 2002; Pauwels et al., 2009; Seo et al., 2011). The JA-induced stress signaling involve multiple signal transduction pathways: (1) stress signal perception and transduction events systemically and locally, (2) induction of JA biosynthesis in response to signal perceived, (3) the perception of JA and activation of defense responses that also integrate with other signaling pathways. Among jasmonates (JAs), JA is well characterized and the most abundant phytohormone in plants. The role of JA signaling in plant defense responses was first reported by Farmer and Ryan (1992). The authors found a causal link between insect/herbivore-induced wounding, JA biosynthesis, and the activation of proteinase inhibitors genes that prevent insect feeding. It is reported that JA-mediated defense responses are induced due to necrotrophic pathogen infection (Avanci et al., 2010). Exogenous application of JA confers improved plant tolerance against pests, which are related to an increase in polyphenol oxidase and proteinase inhibitors activities (Thaler et al., 2001). Similarly, JAs are fundamental in symbiotic interactions, such as arbuscular mycorrhiza, where its colonization in barley leads to the accumulation of JA and trigger plant defense responses during the early stages (Hause et al., 2002; Liu et al., 2003). The induction of JA-induced stress signaling pathways primarily involve the activation of multiple genes such as those encoding plant defensin (PDF1.2), thionin (Thi2.1), and VSPs (vegetative storage proteins) (Epple et al., 1995; Benedetti et al., 1995; Penninckx et al., 1998). In addition to that the transcriptional activation of a MAPK named WIPK was reported within minutes of wounding stress in tobacco (Seo et al., 1995, 1999). The authors found the enhanced accumulation of JA and MeJA in tobacco plants under wounding stress; however, it did not show any response in wipk mutants, indicating the involvement of WIPK in wound-induced JA biosynthesis. Interestingly, the engineered tobacco plants in which the WIPK expression was genetically decreased were reported to accumulate SA and the subsequent activation of the pathogenesis-related protein 1 (PR1) of the SA-induced signaling route (Seo et al., 1995, 1999). Contrarily, the overexpression of WIPK in transgenic tobacco resulted in JA accumulation and the subsequent activation of the PIN2 (proteinase inhibitor 2) transcripts (Seo et al., 1999). The authors concluded that wounding stress in tobacco activates the WIPK transcription, which in turn activates the biosynthesis of JA and reduces SA-dependent signaling. These results were further supported by the evidence, where wounding induced the expression of mitogen-activated protein kinase4 (MPK4) in Arabidopsis within 2
5 minutes after stress. On the other hand, their mutant plants demonstrated enhanced SA accumulation, and the defense-related PR1 gene (Ichimura et al., 2000; Petersen et al., 2000). Furthermore, the mpk4 lack of mutants did not accumulate the JA-induced Thi2.1 and PDF1.2 even after exogenous JA application. By considering the absence of low level SA in plants that could hinder the JA response, the results indicate that the activation of MPK4 promotes JA-induced expression of Thi2.1 and PDF1.2 and simultaneously suppress SA biosynthesis (Niki et al., 1998). Moreover, it is reported that systemic transcriptional response shares significant overlap with wounding responses and local herbivory, thereby suggesting that JA may be crucial to an evolutionary conserved biotic and abiotic stress signaling network. Recent studies reported that JA plays a crucial role in defense

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mechanisms of plants against salt stress (Pauwels et al., 2009; Demkura et al., 2010; Seo et al., 2011; Du et al., 2013), For example, tolerance of soybean seedlings, exposed to salinity stress, was considerably improved by the exogenously applied MeJA (Pauwels et al., 2009; Yoon et al., 2009). Similarly, imposition of salt stress to rice roots increased the endogenous levels of JA and significantly decreased the salinity stress symptoms (Wang et al., 2001a). In another study, Na1 accumulation in shoots of salt-stressed barley plants pretreated with JA was significantly decreased (Walia et al., 2007). At transcriptional level the upregulation of apoplastic invertase, Rubisco (ribulose 1,5-bisphosphate carboxylase/ oxygenase), and arginine decarboxylase were assumed to be probably convoluted in JAmediated salt tolerance of barley plants. Similarly, JAs application, for example, MeJA was also demonstrated to enhance the oxidative damage tolerance of plants under heavy metal toxicity (Maksymiec et al., 2007; Yan et al., 2013). In addition, JA-induced signaling is also described to play key roles in the plant’s development-related processes at several growth stages, for example, flowering and fruiting, secondary metabolism, and senescence (Fahad et al., 2015b,c). Altogether, it is clear that JA-induced signaling regulate the diversity of functions.

16.26 Salicylic acid signaling SA as a signal molecule is a key phytohormone mediating plant defense-related responses against a diverse array of pathogen attacks and response to multiple abiotic stressors, for example, salinity, heat, drought, and osmotic stress (Liu et al., 2016; Lu et al., 2016). Bacterial and fungal plant pathogens are reported to interfere with SA metabolism, signal transduction pathways, and its cross talk with other signaling pathways, by delivering effector proteins to the host cell. However, it remains unclear if these effector proteins could directly bind to SA signaling proteins and/or biosynthetic enzymes to modulate their activities. Moreover, pathogens produced chemical compounds, for example, coronatine (COR) produced by Pseudomonas syringae, that interfere with host signaling pathways (Zheng et al., 2012). COR is structurally similar to JA-Ile and activate JA pathway in host cell, while decreasing the accumulation and signaling induced by SA (Zheng et al., 2012). On the other hand, parallelly to the use of effector proteins and chemical compounds for their own benefit by pathogens, the host cells are also reported to identify certain pathogens among those proteins and chemicals leading to the activation of defense mechanisms against the invaders (Hamdoun et al., 2013). Under pathogen attack the key role of SAinduced signaling pathways includes stimulation of basal defense and resistance genemediated response as well as SAR (systemic acquired resistance) (Liu et al., 2016; Lu et al., 2016). Supplementation of SA is reported to induce SAR and impart stress resistance against pathogen attack at the systemic level. Park et al. (2007) identified methyl SA as its derivative implicated in SAR. Thus transgenic plants impaired in SA accumulation and subsequent signaling were shown to compromise in SAR (Park et al., 2007). During secondary infection, SA is required for SAR-inducing molecules such as azelaic acid. Furthermore, the accumulation of SA in the absence of pathogen infection was reported in the pretreatment of plants with the SAR-related molecule diterpenoid dehydrobietinal (Jung et al., 2009; Chaturvedi et al., 2012).

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SA is able to activate multiple stress-responsive genes encoding antioxidants, HSPs, chaperones, and secondary metabolites, and also SA can involve in the regulation of MAPK pathways, and in the transcriptional stimulation of NPR1 (nonexpresser of pathogenesis-related1) (Jumali et al., 2011; Chai et al., 2014; Herrera-Va´squez et al., 2015). However, the reprogramming of the transcriptional machinery during the abiotic stress response was found to be mediated via SA, where the expression pattern of multiple stress-responsive transcripts can be modulated in a spatio-temporal manner through SA-induced processes (Herrera-Va´squez et al., 2015; Khan et al., 2015). For SA-mediated transcriptional reprogramming, NPR1 is a vital part of one of the signaling pathways that interacts with bZIP TFs in the TGA family (An and Mou, 2011; Yan and Dong, 2014). SA is reported to regulate the expression of NPR1 protein in cell nucleus, by its posttranslational modifications (PTMs) (Tada et al., 2008). In a recent study, two homologs of nucleus-localized NPR1 protein has been identified, namely, NPR3 and NPR4, which control NPR1 activity for ubiquitin-induced degradation of protein under high and low SA, respectively, exhibiting variable SA-association affinities (Fu et al., 2012). But it is still doubtful if NPR1 itself acts as an SA receptor. Nevertheless, intermediate SA levels in the defense zone are required for NPR1 activation during SA signaling (Wu et al., 2012). As a central transcriptional regulator, NPR1 is reported to control about 95% of SAdependent genes in plant pathogen response (Wang et al., 2006; Janda and Ruelland, 2015). On the other hand, it has been shown that SA is involved in plant response to abiotic stressors, and most abiotic stresses increased SA concentration, which also highlights its involvement in stress signaling (Fu et al., 2012; Wu et al., 2012; Lu et al., 2016). In addition to the central role of SA in stress signaling, SA is also reported to integrate with other components of signal transduction pathways such as ROS as well as phytohormones (Lu et al., 2016). Among them the synergistic and antagonistic relationship between JA and SA has been extensively discussed. For instance, thioredoxin (TRX) and glutaredoxin (GRX)-mediated redox status of the cell is reported to depend on cross talk between JA and SA (Yan and Dong, 2014). Similarly, NPR1—the SA transcriptional regulator—is a redox sensor regulated by members of TRX/GRX oxidoreductases, indicating the cross talk between redox signaling, SA and JA. Recent evidence also hints toward the SA and the circadian clock that have profound effect on the growth, development, and environmental stresses responses in plants (Lu et al., 2016). Different research groups reported the circadian clock
mediated control of SA biosynthesis during the daytime, and the SA produced in turn modulates clock activity (Zhou et al., 2015). This integration of SA signaling pathways with other coregulatory pathways highlights the critical role of SA in regulating diverse cellular processes in addition to defense responses. Concluding from the aforesaid, it is clear that SA-induced signaling and its cross talk with the other components of signal transduction pathways play multifaceted roles in plant defense. Therefore it is extremely important to identify new players of this pathway and to further understand the molecular mechanisms involved the integration of SA signaling with other pathways.

16.27 Nitric oxide NO is a small, neutral, and highly diffusible signaling phytohormone that plays a key role in several plant physiological processes, for example, reduction of seed dormancy,

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induction of seed germination, metabolic homeostasis, floral regulation, stomatal movement, photosynthetic processes, mitochondrial functionality, gravitropism, programmed cell death, and increasing tolerance to various abiotic stresses (Beligni and Lamattina, 2000; Pedroso and Durzan, 2000; Takahashi and Yamasaki, 2002; Zottini et al., 2002; Guo and Crawford, 2005; Hu et al., 2005a,b; Bethke et al., 2005; Zheng et al., 2009; Pareek et al., 2009; Kohli et al., 2013; Fancy et al., 2017; Souri et al., 2017). NO as an intra- and extracellular messenger modulates diverse signaling pathways by interacting directly or indirectly with a wide array of cellular targets, thus reprogramming gene expression and modulating protein function (Tuteja and Sopory, 2008; Fancy et al., 2017). The molecular targets of NO, include mitochondrial and chloroplastic proteins, ubiquitously present low and high molecular weight cellular thiols, phenolic groups, amine-containing nucleic acids, iron-containing proteins, membrane-associated lipid radicals and lipoproteins, the TIR1 auxin receptor, outward rectifying K1 channels in guard cells, and ROS (Joshi et al., 1999; Sokolovski and Blatt, 2004; Terrile et al., 2012; Simontacchi et al., 2015). NO accumulation under stress conditions increase and control the transcriptional activation of HSPs (Mata-Pe´rez et al., 2016; Souri et al., 2017). Moreover, NO-dependent modifications of macromolecules, such as nucleic acids, fatty acids, cyclic guanosine monophosphate (cGMP), participate in the complex signaling networks (Freschi, 2013). It is reported that 8-nitro-cGMP synthesis is activated in guard cells by NO, ABA, and ROS, leading to stomatal closure in the light; however 8-nitro-cGMP may represent a new element in the signaling, thereby mediating plant stress
related responses (Joudoi et al., 2013; Asgher et al., 2017).

16.28 NO biosynthesis In animal cells, NO is produced by NO synthases (NOS), oxidizing L-arginine to L-citrulline and NO, and this reaction uses NADPH as an electron donor and super oxide anion (O2 2 ) as cosubstrate (Fig. 16.16) (Mayer and Hemmens, 1997; Wendehenne et al., 2001; Crawford, 2005; Santolini et al., 2017). Surprisingly, an in-depth analysis of numerous plant genome did not identify gene-encoding NO enzymes in land plants, despite the NOS-like activity presence in numerous plant species (Delledonne et al., 1998; Santolini et al., 2017). NO3– NADP, H2O

NADPH, O2

NOS L-Arg

NR Cenillurti

NO2–

NO

Ascorbic acid

FIGURE 16.16

NR

Carotenoids

A schematic representation of the NO biosynthesis pathway.

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The reduction of nitrate-by-nitrate reductase (NR), followed by nitrite reduction into NO by NR itself or via the mitochondrial electron transport chain is one of the most important sources of NO in land plants in the absence of functional NOS proteins (Crawford, 2005; Gupta et al., 2011; Fancy et al., 2017). In addition, other potential enzymatic candidates, such as xanthine oxidase, cytochrome P450, and copper amine oxidase 1, have also been reported as potential NO production sources in plants (Asgher et al., 2017). Alternatively, nonenzymatic sources include the reduction of nitrate to NO by carotenoids and phenolic compounds such as ascorbic acid (Fig. 16.16) (Bethke et al., 2005; Crawford, 2005; Asgher et al., 2017).

16.29 NO signaling NO mediates multiple plant physiological processes and other stress response characteristics (Singh et al., 2016). It regulates various plant biological processes by directly modifying proteins by PTMs giving rise to S-nitrosylation, nitration, and nitrosylation or indirectly by regulating gene transcription (Romero-Puertas and Sandalio, 2016). The Snitrosylation of cysteine residues regulated NO-dependent PTM has emerged as crucial mechanism intermediating NO-dependent signal transduction in plants, which is subsequently implicated in regulating the functions of various components of plant processes as various as protection against oxidative stress, photosynthesis, cellular architecture, genetic information processing, and defense responses to abiotic stresses and hormonal signaling (Astier et al., 2012; Freschi, 2013; Romero-Puertas and Sandalio, 2016). In addition, another main NO-dependent PTM involves NO binding to central position in metalloproteins in a process called metal nitrosylation, which is the activation of cGMP and important intermediate in multiple NO-induced processes such as defense responses (Fig. 16.17) (Pagnussat et al., 2002; Freschi, 2013). The key feature recognized in plant NO-dependent signaling is the PRM of S-nitrosylation (Kovacs and Lindermayr, 2013), which can modify enzymatic activity or block the PTMs regulatory sites and therefore effect signaling pathways, also including those of ABA, for example, SnRK2 nitrosylation, CK (nitrosylation of ARRs), and AUX (nitrosylation of TIR1 receptor), which leads to an increased hormone
receptor interaction and enhanced AUXdependent transcript expression (Feng et al., 2013; Terrile et al., 2012; Wang et al., 2015b). On the other, NO can interact with reduced GSH to produce GSNO (S-nitrosoglutathione) (Fig. 16.17), which can be subsequently converted to GSSG (oxidized GSH) and NH3 by the enzyme GSNOR (GSNO reductase) (Leterrier et al., 2011; Souri et al., 2017). GSNO, as a mobile reservoir of NO bioactivity, can modulate cellular signaling pathways through specific PTMs of redox-modulated proteins by a reaction of transnitrosylation, whereby GSNO can transfer NO to Cys residues of proteins (Corpas et al., 2013). The GSNO stability is dependent on the presence of other compounds, such as ascorbate (ASC) and GSH, which can decompose GSNO to generate NO and GSSG (Smith and Marletta, 2012; Corpas et al., 2013). Furthermore, GSNO—representing a highly stable intracellular NO reservoir—can be transported to other tissues and cells, where it can be removed via GSNOR or cleaved into GSH and NO, or its NO group can be directly transported to other cellular thiols via S-transnitrosylation reactions (Asgher et al., 2017). It has recently been demonstrated that GSNOR activity is critical for AUX transport and signaling (Shi et al., 2015).

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FIGURE 16.17

A model of the NO signaling pathway.

Since during abiotic stress, maintain the balance of water in cells and the regulation of function guard cells are very important, the function of NO as a secondary messenger in guard cells thus holds great significance, and NO functions as an important intermediate during the ABA-induced signaling network regulating stomatal closure. NO and H2O2, as signaling molecules, act in guard cells, and it is evident in the cells that these signaling molecules can mediate ABA-mediated stomatal closure by Ca21 channels, c-GMAP, cADPR, and MAPKs (Fig. 16.17) (Pei et al., 2000; Joudoi et al., 2013). The exposure of plants to water deficiency induced by different abiotic stresses (drought, salinity, and heavy metals), the loss of cell turgor triggers the biosynthesis of ABA, which enhances NO biosynthesis inside the guard cells and NO generation is important for ABA-persuaded stomata closure (Neill et al., 2002; 2008). Besides, ABA activates H2O2 the generation by NADPH oxidase as important modulators of ROS generation in ABA signaling, and then H2O2 acts in stimulating calcium-permeable channels and thus induces the release of calcium from intracellular stores and influx across the cell membrane (Pei et al., 2000; Kwak et al., 2003; Cho et al., 2009) In the presence of abiotic stressors the generation of redox-active molecules, for example, ROS and RNS (reactive nitrogen species), are the most ubiquitous response

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(Mittler, 2002). Nevertheless, excessive ROS and/or RNS accumulation can lead to cellular oxidative damage, so based on this matter, the regulation of plant redox homeostasis is a crucial aspect of abiotic stress response (Grant and Loake, 2000; Fancy et al., 2017). Increasing evidence suggests that NO functions as a chain-breaking antioxidant-arresting lipid peroxidative reactions and induces antioxidant enzymes at transcript level (Siddiqui et al., 2011; Singh et al., 2009; Hasanuzzaman and Fujita, 2013; Wany and Gupta, 2018). Indeed, NO acting as a direct scavenger of ROS would take over functions of the antioxidant system, and it is as well as inducer of the antioxidant system which would trigger antioxidant gene expression or activate antioxidative enzymes (Fig. 16.17). Exogenous NO was thought to attenuate oxidative stresses by reducing the H2O2 content and by increasing the antioxidant enzymes activity, for example, APX, CAT, GR, POD, and SOD (Singh et al., 2009; Farnese et al., 2013; Souri et al., 2017). Under plans exposure to metal toxicity, it has been considered that NO can stimulate the entire phytochelatins (PC) biosynthetic pathway (Fig. 16.17), because NO may be involved in gene regulation of carriers sulfate and is able to increase the uptake of this ion (Farnese et al., 2013; Singh et al., 2016). Likewise, NO is also able to bind Cys residues of PCs; S-nitrosylation of PCs might reduce the efficiency of heavy metal detoxication (Elviri et al., 2010; Locato et al., 2016; Souri et al, 2017). Since one of the main tolerance strategy of plant to heavy metals is achieved by increasing chelation with PCs (Souri et al, 2017), it seems that NO can be the key role related to PC biosynthetic pathway and S-nitrosylation of PCs.

16.30 Strigolactones SLs as new class of plant hormones are carotenoid-derived signaling compounds, which regulate plant growth and development-related processes. SLs were primarily identified as signal molecules in rhizosphere, involved in symbiotic and parasitic interactions between parasitic seeds/fungi and plant roots (Zhang et al., 2015; Marzec, 2016). They are also involved in plant branching, root development regulation, leaf senescence, and responses to stress (Marzec et al., 2013; Koltai and Kapulnik, 2014; Yamada and Umehara, 2015; Marzec, 2016; Sun et al., 2016a,b). The breakthrough of SLs discovery provided exciting opportunities to understand hormonal modulation of plant developmental and adaptability to environmental stresses (Saeed et al., 2017). It is recently demonstrated that SLs function as an activator of diverse ABA-dependent signaling pathways by controlling the ABA-responsive genes expression and/or transcription of stress-responsive transcripts involved in plant’s developmental and stress-response characteristics (Ha et al., 2014). It has been reported that SL signaling is involved in plant reactions to N/P deficiency stress and also have a role in the regulation of different abiotic stresses such as drought, salinity, and chilling (Jamil et al., 2011; Mayzlish-Gati et al., 2012; Yoneyama et al., 2012; Pe´ret et al., 2014; Saeed et al., 2017; Cooper et al., 2018). The results of new studies indicate the use of genetic engineering as a viable strategy to increase the plant stress tolerance by manipulating SL biosynthesis and/or signaling (Ha et al., 2014; Saeed et al., 2017).

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All-trans- β-Carotene D27

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FIGURE 16.18 A schematic representation of the SL biosynthesis pathway. SL, Strigolactone. Source: Modified from Mishra, S., Upadhyay, S., Shukla, R.K., 2017. The role of strigolactones and their potential cross-talk under hostile ecological conditions in plants. Front. Physiol. 7, 691.

16.31 Strigolactone biosynthesis SLs are sesquiterpene lactones and their chemical structural characteristics are very similar to isoprenoids/terpenoids, suggesting that SLs are carotenoid derivatives (Pandey et al., 2016). SLs biosynthesis is catalyzed by two carotenoid cleavage dioxygenases (CCDs) and a carotenoid isomerase that transform all-trans-β-carotene into carlactone (CL) (Fig. 16.18) (Alder et al., 2012; Marzec, 2016). The enzyme CCDs catalyze the oxidative breakdown of the double bond in 9-cis-epoxycarotenoids, and the primary biosynthesis reaction occurs in the chloroplast with the help of three enzymes Dwarf27 (D27), CCD7 and CCD8 (Fig. 16.18) (Booker et al., 2005; Mishra et al., 2017). Following SLs transport into the cytoplasm, more axillary growth1 (MAX1) (Fig. 16.18), a cytochrome P450 monooxygenase convert CL into carlactonic acid, which is subsequently transformed into orobanchol or 5-deoxystrigol, two main precursors of other SLs (Cardoso et al., 2014; Seto et al., 2014; Marzec, 2016). Subsequently, SLs or their precursors are transported to shoots or might be exported into the root zone by the ABC type transporters (Prandi and Cardinale, 2014). ABA is a modulator of biosynthesis of SLs, and it can act as suppressor for different carotenoid cleaving enzymes (Peleg and Blumwald, 2011).

16.32 Strigolactone signaling Similar to other the phytohormones (AUX and GA), SL signaling mechanisms are accomplished by proteosomal degradation (Figs. 16.5, 16.11, 16.19). It has been shown to

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FIGURE 16.19 An overview of the SL signaling pathway. SL, Strigolactone. Source: Modified from Li, W., Tran, L.S., 2015. Are karrikins involved in plant abiotic stress responses?. Trends Plant Sci. 20, 535
538; Wang, L., Wang, B., Jiang, L., Liu, X., Li, X., Lu, Z., et al., 2015a. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27, 3128
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the F-box protein MAX2 that acts as a recognition subunit in an SCF-type (SKP1-CUL1-Fbox-protein) ubiquitin ligase complex, be prerequisite for the SL response (Fig. 16.19) (Mishra et al., 2017). The machinery signaling of SL comprises the α/β-fold hydrolases called DAD2/D14/RMS3, the F-box leucine-rich protein D3/MAX2/RMS4 (Stanga et al., 2013; Saeed et al., 2017). The SL receptors include D14 and DAD2, which are the members of the α/β-hydrolases family (Nakamura et al., 2013). With attaching SL molecule to D14/ DAD2, occur a change of the D14/DAD2 conformation, that is fundamental for the interaction of theses protein by other constituents of the SL signal transduction pathway (Nakamura et al., 2013; Zhao et al., 2015; Marzec, 2016). During SL signaling the central element is SCF, and the perception of SL inducts identification and binding of target proteins through F-box proteins that are later bound via Skp1, before Cullin, the core structural part of SCF complex, links the complex to ubiquitin ligase (Nakamura et al., 2013; Marzec, 2016). In following this step the protein recognized through the F-box protein is ubiquitinated and consequently go under proteasomal degradation (Fig. 16.19) (Marzec, 2016). Therefore the proteasome-induced degradation of the repressor via SCF complex is a recognized process of SL-induced gene expression (Wang et al., 2015a). SL, loaded with the D14 SL, is then employed to SCFMAX2 that is able to direct further the proteosomal dissociation of the targeted proteins (Fig. 16.19) (Jiang et al., 2013; Zhao et al., 2015). The D53 as first SL repressor is identified from rice, and also lately in A. thaliana, three orthologous of D53 recognized were reported to negatively regulate in SL signal transduction pathways and called Suppressor of MAX2-like 6
8 (SMXL6
8) (Zhou et al., 2013a; Wang et al., 2015a; Soundappan et al., 2015; Marzec, 2016). Members of the SMXL/D53 family encompass EAR (ethylene-responsive element binding factor-associated amphiphilic repression) domains, which were previously reported to regulate interaction with Topless (TPL) family members of the transcriptional cosuppressors that participate in pathways of plant developmental and phytohormonal signaling (Causier et al., 2012; Smith and Li, 2014). D53 is able to react with the transcriptional cosuppressor TPR

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(TPL-related), and subsequently the TPR-D53 complex negatively regulate the transcriptional expression of the targets of SL activity (Smith and Li, 2014; Soundappan et al., 2015). While the SMXL/D53 family has not been reported to involve in reactions to the other signals, TPR-proteins are reported to involve in response to various other types of signals and development response
related processes (Smith and Li, 2014). This renders an opportunity for cross talk and integration of SL signaling with other signaling systems in the gene expression control and plant development (Smith and Li, 2014; Saeed et al., 2017).

16.33 Karrikins

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KAR is a planar compound derivative from burning plant material, which imparts a crucial role in several biological processes such as germination regulation, seed dormancy release, inhibition of hypocotyl elongation, seedling establishment, seedling vigor enhancement under stressful environments (Flematti et al., 2013; Smith and Li, 2014; Li and Tran, 2015). The original parent of KAR molecule is denoted as KAR1, in recognition of its lactone structure (analogous to BL) (Li and Tran, 2015; Flematti et al., 2013). KARs are quite similar to SL in both chemical structure and signaling transduction pathways. Recent reports have revealed that SL play a positive role in plant responses to salt and drought stress via MAX2, which is a mediator between SL and KAR signaling (Figs. 16.19 and 16.20) (Li and Tran, 2015). KAR action requires the MAX2 (an F-box protein) and the α/β-hydrolase KAR insensitive2 (KAI2), a paralogue of D14 that is essential for SL perception. MAX2 plays a main role in drought and salinity stress adaptation (Waters et al., 2013; Ha et al., 2014; Liu et al., 2015; Li and Tran, 2015).

TFs

The expression of KR-response genes

FIGURE 16.20 An overview of the KR signaling pathway. Source: Modified from Li, W., Tran, L.S., 2015. Are karrikins involved in plant abiotic stress responses? Trends Plant Sci. 20, 535
538; Wang, L., Wang, B., Jiang, L., Liu, X., Li, X., Lu, Z., et al., 2015a. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27, 3128
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16.34 Karrikin signaling KAI2 as the α/β-hydrolases is the receptor in KARs signaling pathway (Waters et al., 2013). MAX2 and KAI2 (with similar structure to D14), are essential for the KAR responses. Similarity, in SL signaling, a protein called SMAX1 (suppressor of MAX2 1), was known as a negative regulator of KAR signaling, and there are the similar perception mechanisms and possibly cross talk between KAR and SL signal transduction pathways via the mediator MAX2 (Fig. 16.20) (Stanga et al., 2013; Li and Tran, 2015). KAR signal transduction also involves F-box protein MAX2 and KAI2 (Fig. 16.20) (Bythell-Douglas et al., 2013). When KAR binds to KAI2, inducing a protein conformational change, which potentially allows MAX2 to interact with KAI2, the F-box subunit of an SCF class of E3 ubiquitin
protein ligase complex (Zhao et al., 2013). MaX2/KAI2 is thought to function in an SCF complex that tags transcriptional activator for degradation (Fig. 16.20). Analogous to DELLA protein manner in GA signaling, it is supposed for the determinations of this model that these partner proteins are negative regulators of growth and are targeted for ubiquitin-mediated degradation by SCFMAX2 (Zhao et al., 2013). Afterward, KARs and KAI2 might form an SCF E3 ligase complex with MAX2 (Waters et al., 2013). The SCF complex is able to promote the degradation of SMAX1, which is a repressor in KARs signaling pathway (Fig. 16.20) (Stanga et al., 2013). Based on a genetic study of SL deficient Arabidopsis mutants, that is, max3 and max4 in Arabidopsis, SL plays a vital role in the modulation of abiotic stressors, for example, drought and salt stress, and also has been revealed that the SL signaling member MAX2 plays a crucial role in stress adaptation (Ha et al., 2014). Therefore given that MAX2 be a fundamental point of cross talk between the SL and KAR signal transduction pathways, it has been advocated that KAR can play role that is related to ABA in mediating plant adaptive response mechanisms to abiotic stressors (Ha et al., 2014; Li and Tran, 2015).

16.35 Cross talk between phytohormone signaling In the past decades, studies using a variety of plant phenotypes, including plants bearing mutations in hormone-biosynthetic pathways, provided clear evidences of hormonal cross talk, either synergistic or antagonistic, by which hormone biosynthesis and responses are modulated (Santner and Estelle, 2009; Peleg and Blumwald, 2011; Wang and Irving, 2011). Such cross talk has been demonstrated to affect hormonal balance, playing key roles at the whole plant physiology level, and it is now evident that physiological processes, such as various responses to stressful conditions, are regulated in a complex way through the cross talk of various hormones (Peleg and Blumwald, 2011; Munne´-Bosch and Mu¨ller, 2013). Interactions among the biosynthetic pathway of hormones have been recently demonstrated. For example, ABA has been suggested as playing roles on SLs, CK, and NO biosynthesis. Based on SLs biosynthesis and their physiological role in plants directed to well-known detail, SLs need to regulate and react with several hormones, in particular ABA and AUX to exercise their effect, and recent findings suggest that SL and cross talk of it with other hormones are crucial players of growth optimization in response to

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environmental stressors (Saeed et al., 2017). The genes responsible for regulating SLs biosynthesis are closely associated with NCED gene family members that are directly involved in biosynthesis of ABA, and both ABA and SLs derive from the same precursor, that is, carotenoids. Hence, the two biosynthetic pathways are interdependent (Lo´pezRa´ez et al., 2010). Exogenous ABA was also demonstrated to strongly downregulate the key gene involved in the CK biosynthesis, that is, IPT, and upregulate the genes that encode CK dehydrogenases and oxidases (Nishiyama et al., 2011). This last study also highlighted a mutual regulation mechanism between ABA and CK regarding diverse processes of stress adaptation. Finally, NO has been further demonstrated to be accumulated in guard cells of a number of species in ABA response (Desikan et al., 2002; Garcia-Mata and Lamattina, 2007). Interactions between ABA and BR modulate the expression of numerous genes, which manage many biological processes, for example, seed germination, stomatal closure, environmental stresses response, and overall plant growth
related responses (Steber and McCourt, 2001; Haubrick et al., 2006; Kagale et al., 2007; Acharya and Assmann, 2009; Choudhary et al., 2012). Both BR and ABA apply a stimulating impact on stomatal closure that is possibly mediated through NO working as the regulator of ABA-dependent stomata closure (Zhang et al., 2010). By mediating the growth and developmental responses to various abiotic stresses, hormonal cross talk has been proposed to define plant tolerance to a number of stresses (Peleg and Blumwald, 2011; Verma et al., 2013, 2016). During both air and soil water deficit, plants can rapidly reach lower water potentials, and stomatal closure is then a key mechanism to reduce transpiration, maintaining plant hydration (Brodribb and McAdam, 2017). Drought-induced stomatal closure in angiosperms is mediated by the phytohormone ABA. More recently, however, other studies suggested that other plant hormones, for example, BR, CK, ET, SA, JA, and NO can interact with ABA, affecting stomatal movement. BR, SA, ABA, JA, and NO are proposed to drive stomatal closure under drought (Acharya and Assmann, 2009). For instance, CK levels decline under water deficit, while ABA levels increase, leading to stomatal closure (Pospisilova et al., 2005). Another example is the NO requirement for stomatal closure to occur in turgid leaves of A. thaliana (Garcia-Mata and Lamattina, 2002; Ribeiro et al., 2009). On the other hand, CK and IAA have been shown to induce increases in stomatal conductance (Pospisilova et al., 2005; Acharya and Assmann, 2009). There is an interaction between GA and BR, and it has been suggested that OsGSR1, a GA-stimulated transcript (GAST) gene family member, plays crucial roles in both pathways of GA and BR signaling and also regulates their association (Wang et al., 2009). Exogenous GA3 application mediated enhanced expression profiles of NPR1 and ICS1 genes, components of the biosynthetic pathways of SA, and its action, respectively, and overexpressing a GA-responsive gene showed enhanced tolerance under abiotic stresses, and the tolerance was associated with enhanced endogenous levels of SA (Alonso-Ramı´rez et al., 2009; Peleg and Blumwald, 2011). Furthermore, to JA, ICE1 interacts with SAdependent pathways cross talk between SA and JA-mediated signaling pathways to minimize the harmful impacts of chilling stress (Cooper et al., 2018). Under drought, salt, and nutrient-stress conditions, root development and architecture are critical aspects defining plant tolerance (Benkova and Hejatko, 2009; Kohli et al., 2013).

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In this regard, recent studies have demonstrated the epistatic role played by AUX and ET in regulating root development and architecture in abiotic stress response such as boron deficiency (Wang et al., 2013a; Verma et al., 2016). ET is proposed to limit lateral root development, while inducing adventitious root formation via the modification of AUX transport. Further studies demonstrate how these plant hormones impact the development of new and present lateral roots and root cell expansion (Strader et al., 2010), and others show how the interaction between AUX and ET also plays roles for apical hook production in A. thaliana seedlings (Wang et al., 2013a). Light shortage is another critical stress that suppresses plant growth and development. Shade often results in dim light intensity along with dim blue light intensity and a lower ratio of red/far-red. Together, such environment can induce SAS (shade avoidance syndrome) that is mostly defined by a fast stem elongation and a transient reduction of leaf growth. Studies on mutant screening for SAS response have shown that AUX, CK, GA, BR, and ET are involved in regulating SAS phenotype (Kanyuka et al., 2003). Shaded leaves accumulate AUX that is next transported to the hypocotyl to interact to GA and other hormones, leading to the rapid stem elongation observed in SAS. AUX is also responsible for inducing CK catabolism in developing leaves resulting in leaf growth inhibition, and this result indicates that the hormonal cross talk underpinning SAS is organdependent (Carabelli et al., 2007; Kohli et al., 2013). While drought stress remains the best studied stress regarding hormonal cross talk (Peleg and Blumwald, 2011), information on other stressors, such as under salt, flooding, and heavy metal conditions, are documented to a limited extent (Bailey-Serres and Voesenek, 2010; Ghanem et al., 2010; Xu et al., 2010, 2011b). Revealing additional interaction processes among plant hormones resulting in growth and development regulation under various growth-limiting conditions is a significant theme in the field of abiotic stressors, providing new information for genetic improvement of crop plants challenged by global climate change (Verma et al., 2013, 2016). On the other side, in related phytohormonal signaling, plants encountered with abiotic stress conditions develop efficacious defense systems by the cross talk among the endogenous signaling molecules, such as hormones and secondary messenger such as Ca21 and H2O2. In cross talk signaling network, phytohormones contribute the main role in improving adaptability of plants under changing environment (Kundu and Gantait, 2017). Phytohormones make a network of signaling and mutually regulate various metabolic and signaling systems, which are vital for abiotic stress responses (Munne´-Bosch and Mu¨ller, 2013). During abiotic stress the abiotic stress perception prompts the stimulation of signaling cascades, which react with the baseline pathways transmitted via phytohormones, and the cross talk between phytohormones and the signaling network activate either a secondary messenger or a phosphorylation event via kinase cascades as cross talk points in hormonal networks (Harrison, 2012). The variations of stress-responsive phytohormones assist changing cellular dynamics and therefore play a key role in coordinately modulating growth response under stress environments (Kohli et al., 2013). The awareness of cross talk between phytohormonal signaling can present useful evidence on the convoluted method of plant stress adaptability that would support to improve plants-stress tolerance. Plant cell dehydration is a consequence of various abiotic stresses, and also microarray studies have characterized significant data of overlapping transcript expression related to

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abiotic stressors, which involve drought stress (Harrison, 2012). When plant exposer to osmotic stress, such as drought and dehydration, is perceived through a specific HK osmoreceptor, which is expressed at an upper level (Wohlbach et al., 2008). It has also been suggested that HK1 is an activator of the osmotic stress
induced response and prompts several downstream targets, those including enzymes of biosynthetic pathways of ABA and ABA-responsive TFs (Wohlbach et al., 2008). Moreover, as previously mentioned, there is an interaction between phytohormonal signal transduction pathways in ABA-mediated stomata closure as a consequence of osmotic stress, and it has been suggested that other plant hormones such as AUX, BR, CK, ET, JA, NO, and SA also impact stomata function (Neill et al., 2008). While BR, ABA, JA, SA, and NO mediate stomata closure, AUX and CK stimulate stomata opening (Acharya and Assmann, 2009; Peleg and Blumwald, 2011). Indeed, CK and AUX inhibit ABA-induced stomata closure by increasing ET production, which decreases the level of H2O2 in guard cells and finally suppresses stomata closure responses (Tanaka et al., 2006; Song et al., 2012). It was also reported that the AUX treatment can enhance EIN3 protein accumulation in an EIN3-binding F-box protein1-(EBF1)-dependent manner, that indicates a significant point for ET and AUX signal cross talk (Kohli et al., 2013). In relation to cross talk between ABA and JA, a JA-induced stomata closure in A. thaliana has been noted, and a linking between the ABA receptor NtPYL4 is also recognized that is involved in main ABA-induced signaling and JA-dependent responses during optimizing the trade-offs between plant growth and response to stresses in order to adaptation (Hossain et al., 2011). The signal of osmotic stress prompts an increment in the ABA levels in guard cells, where it binds to its receptor, in which SnRK2 is promoted by phosphorylation (Harrison, 2012). On the other hand, H2O2 and NO as secondary messenger triggers the influx of Ca21, which activates CDPKs that activate anion efflux and prevent K1-influx, and the consequent ion loss results in water efflux, loss of turgor pressure, and finally stomata closure (Neill et al., 2008; Kim et al., 2010; Harrison, 2012). Besides, H2O2 has a main role as signaling molecules participating in the complex network regulating cell response to abiotic stress, which also include NO, phytohormones, and MAPK signaling cascades. It has also been suggested that JA reacts with ABA-mediated stomata closure through inducing the influx of extracellular calcium and/or by activating NO/H2O2 signaling, but contrastingly, it has been proposed that stomata closure through ET is modulated via its signal transducing pathways, which both promotes generation and entails H2O2 production (Desikan et al., 2006; Harrison, 2012). This cross talk also involves JA, and its biosynthesis is prompted under several stressful conditions such as drought stress, where JA binds with ABA-mediated stomatal closure through increasing calcium influx, that ultimately activates CDPKs and the resulting signaling cascade (Huang et al., 2008; Harrison, 2012; Wani et al., 2016). MAPK-mediated pathways are versatile, and common signaling components, which lie downstream of secondary messengers and phytohormones, play crucial roles under variable environmental conditions (Raja et al., 2017). The MAPK signal transduction activity signifies a vital role of MAPK cascade during ABA-dependent signal transduction pathways (Fig. 16.3), and it has been suggested that MAPK-dependent pathways modulate numerous ABA responses such as antioxidative defense in order to alleviating oxidative

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damage, which is created by abiotic stresses (Zong et al., 2009; Danquah et al., 2014). The various kinds of MAPK can be triggered by abiotic stresses, such as salinity and drought, and also hormone stimulus (Taj et al., 2010; Kundu and Gantait, 2017). It has been demonstrated that, in rice ABA regulate the transcript levels of numerous MAPKs, such as OsMAPK2, OsMAPK5 (OsMAP1), OsMAPK44, OsMSRMK2, OsMSRMK3, OsBIMK1, OsWJUMK1, OsEDR1, OsSIPK, DMS1, and OmMKK1, and in maize has reported ZmMKK3 in ABA-responsive osmotic stress, and in Arabidopsis triggered the transcript level control of many MAPK types, for example, MPK3/5/7/18/20, MKK9, MAPKKK1/ 10/14/15/16/17/18/19, and Raf6/12/35 suggesting a significant role in ABA-dependent signal transduction (Ding et al., 2009; Wang et al., 2011; Danquah et al., 2014; Kundu and Gantait, 2017). In addition, the transcription of ZmMPK17 is responsive to plant hormones, for example, ABA, ET, SA, and JA under extreme temperatures, drought, and salinity stress, and the overexpression of ZmMPK17 caused the reduction oxidative stress by affecting the process of antioxidant production (Pan et al., 2012). There is a molecular level link between AUX-dependent signaling and oxidative damage, and it has been showed that ROS formation during abiotic stressors alters AUX gradients that in response reduce AUX-mediated signal transduction (Raja et al., 2017). The interaction of redox metabolism and AUX signaling mediated the adaptive responses against abiotic stress such as salinity, heavy metals, or oxidative stress (Iglesias et al., 2010). In agreement with this hypothesis the tir1afb2 mutants, the double mutant for TIR1-AFB2 AUX receptors, exhibited reduced ROS accumulation, enhanced antioxidative activity, and was also more resistant to abiotic stresses such as salinity than the wild type plants (SalopekSondi et al., 2017). The adaptation to salinity speculated to be mediate, might be partly, by AUX/redox interaction. It can be concluded that the cross talk between AUX and the redox metabolism mediating as a new regulatory mode through which plants regulate growth and development responses including adaptation responses to stressful environments. AUX, ROS, and antioxidant compounds ASC, reduced GSH, PCs, and related proteins are suggested as forming a redox-signaling module which links plant growth responses with environmental signals (Tognetti et al., 2012; De Tullio et al., 2010). Small regulatory RNAs or microRNAs (miRNAs) are other ubiquitous signaling molecules mediating signal transductions during abiotic stress that regulate posttranscriptional gene expression. Some of these miRNAs are reported to act as AUX signaling component (Sanan-Mishra et al., 2013). For instance, miRNA393, miRNA402, and miRNA397b, which have emerged as encoding AUX receptor TIR1, demeter-like protein3, and LACCASE, respectively, are upregulated in Arabidopsis, rice, maize, and Phaseolus vulgaris in response to abiotic stressors such as cold, dehydration, and salt stress (Salopek-Sondi et al., 2017). In Arabidopsis, mutant analysis indicated that HKs as CK receptor negatively regulate ABA and osmotic stress
dependent signaling, whereas AHK1 regulates positively the similar processes (Tran et al., 2007; Kohli et al., 2013). Moreover, after dehydration AHK2 is upregulated, and AHK3 production is promoted via several abiotic stresses, and ahk2 and ahk3 mutants improved tolerance to salt and drought stress, which shows that AHK2/3 negatively regulate the osmotic stress responses (Harrison, 2012). Therefore CK is also reported to be involved in stress signaling and the HKs play crucial roles in ABA and CK cross talk in relation to stress-dependent signaling (Tran et al., 2007; Kohli et al., 2013).

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In regulating the stress responses the principal roles played by GA and ABA are obvious from the interfaces surrounding DELLA proteins, which create main cross talk with AUX, ET, and JA, and it has also been indicated that the cross effects between ET, SA, and JA signaling pathways play essential roles in plant defense mechanisms (Wang and Irving, 2011; Wang et al., 2013b; Riemann et al., 2015). In general the interplay of environmentally activated classical phytohormones including ABA, ET, CK, and GA signals primarily defines plant responses to different stressors (Achard et al., 2006; Qin et al., 2011b; Kohli et al., 2013). NO and AUX signaling pathways are intricately interconnected during the regulation of several plant responses (Chen et al., 2010; Sanz et al., 2015). In the signaling pathway, NO interaction with AUX involves the regulation of CDPK activity, which doing as downstream messengers prompted by AUX (Pagnussat et al., 2002; Asgher et al., 2017). There is a positive cross talk between AUX and NO during heavy metals stress, and it has been showed that GSNOR activity, which mediates denitrosylation processes, is crucial for AUX signaling (Xu et al., 2011a; Shi et al., 2015). In stress responses, there is a key role for BR, and the importance of H2O2 and antioxidant responses in the BR action and its involvement in conveying environmental stress has been underscored. Moreover, the combined action of ABA, BR, and NO during oxidative stress tolerance was documented (Zhang et al., 2010; Hao et al., 2013). There is a possible link between CK and BR signal transduction pathways, and CKs concurred with the upregulation of many BR-related transcripts, for example, DWF5, BAK1, SERK1, and BSK1, indicating that cross talk between CKs and BRs can contribute to the modification of source/sink relations and lead to improved drought stress tolerance (Choudhary et al., 2012; Hayat et al., 2012). The cross talk between SA and BRs play a key role during response to abiotic stressors (Wani et al., 2016; Sharma et al., 2017). BR-mediated salt tolerance in A. thaliana somewhat depends on NPR1 (a master regulator of the SA-induced stress signaling pathways) (Divi et al., 2010). It has also been shown that the combinatorial application of BRs and SA is most effective in reducing salinity stress (Hayat et al., 2012; Choudhary et al., 2012). In related to NO actions, it has been shown that the expression of transcripts in response to NO mediate through JA and SA signaling pathways (Gru¨n et al., 2006). During the regulation of responses against abiotic stress, both of NO and SA show synergistic or antagonistic relationship, and it has also been indicated that SA-induced protein kinase might work downstream of SA in the NO-dependent signaling pathway (Durner and Klessig, 1999; Asgher et al., 2017). There is an indication for the association of SL signaling with BR and GA signaling resulting from searching proteins that bind to MAX2/D3 and D14 (Smith and Li, 2014). In rice, D14 displays an SL-dependent binding to SLR1 (a DELLA protein), indicating a strategy for the close coordination of GA and SL signaling (Nakamura et al., 2013). It has been shown that BR-activated TF BES1 binds to MAX2 and is targeted for dissociation by SL-stimulated binding to D14, so MAX2 is also involved in the BES1 degradation (Wang et al., 2013b; Smith and Li, 2014). Also, the role of SLs and ABA in regulating the development of root via interaction with AUX and ET has also been defined, which lead to abiotic stress tolerance such as salt, drought, and nutrient deficiency stress (Kohli et al., 2013).

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The investigation of phytohormonal signaling suggest that their signaling can help as prospective objectives for genetic engineering of plants with enhanced tolerance against abiotic stressors, and the activation of selective phytohormonal signaling components through biotechnological approaches increases plants tolerance. Thus the characterization of signaling pathways and genes is involved in each pathway for the production of transgenic plants with improved abiotic stress tolerance. Recent advancements in molecular biology and genetics have enabled the identification of several complex signaling networks that contribute to abiotic stress responses (Joshi et al., 2018). Since phytohormones target numerous members of proteins families that play significant roles in plant growth either individually or in a coregulated manner, biotechnological manipulation of the targeted key proteins could allow better adaptability under hostile growth conditions (Nguyen et al., 2016; Joshi et al., 2018). Meanwhile, there is knowledge gap related to the mechanisms for phytohormonal signaling and their cross talk in plants, yet it should be studied in depth in order to understand these mechanisms to abiotic stresses. Concluding from the previous discussion, all such findings enable us to devise a hypothetical model, where the adaptive response to abiotic stressors appears to be arbitrated in part, via the positive or negative regulation of phytohormones. Identification of plant growth and development response
related programs are crucial to enhance plant survival under stressful environments. Future research will explain the complicated mechanisms that plants adopt to develop such highly dynamic responses.

Acknowledgment We thank Amanda A. Cardoso (Department of Botany and Plant Pathology, Purdue University, West Lafayette, United States) for commenting and improving some parts of this chapter.

References Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D., Shinozaki, K., 1997. Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. Plant Cell 9, 1859
1868. Abeles, F., Morgan, P., Saltveit, Jr, M., 1992. Ethylene in Plant Biology. Academic, New York. Achard, P., Genschik, P., 2009. Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J. Exp. Bot. 60, 1085
1092. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., et al., 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91
94. Achard, P., Baghour, M., Chapple, A., Hedden, P., Van Der Straeten, D., Genschik, P., et al., 2007. The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc. Natl. Acad. Sci. U.S.A. 104, 6484
6489. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., Genschik, P., 2008a. The cold-inducible CBF1 factordependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20, 2117
2129. Achard, P., Renou, J.P., Berthome´, R., Harberd, N.P., Genschik, P., 2008b. Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr. Biol. 18, 656
660. Achard, P., Gusti, A., Cheminant, S., Alioua, M., Dhondt, S., Coppens, F., et al., 2009. Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr. Biol. 19, 1188
1193. Acharya, B.R., Assmann, S.M., 2009. Hormone interactions in stomatal function. Plant Mol. Biol. 69, 451
462.

Plant Life under Changing Environment

444

16. Phytohormonal signaling under abiotic stress

Agrawal, G.K., Tamogami, S., Iwahashi, H., Agrawal, V.P., Rakwal, R., 2003. Transient regulation of jasmonic acid-inducible rice MAP kinase gene (OsBWMK1) by diverse biotic and abiotic stresses. Plant Physiol. Biochem. 41, 355
361. Ahammed, G.J., Choudhary, S.P., Chen, S., Xia, X., Shi, K., Zhou, Y., et al., 2012. Role of brassinosteroids in alleviation of phenanthrene
cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J. Exp. Bot. 64, 199
213. Ahammed, G.J., Li, X., Xia, X.-J., Shi, K., Zhou, Y.-H., Yu, J.-Q., 2015. Enhanced photosynthetic capacity and antioxidant potential mediate brassinosteroid-induced phenanthrene stress tolerance in tomato. Environ. Pollut. 201, 58
66. Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., et al., 2012. The path from b-carotene to carlactone, a strigolactone-like plant hormone. Science 335, 1348
1351. Alonso-Ramı´rez, A., Rodrı´guez, D., Reyes, D., Jime´nez, J.A., Nicola´s, G., Lo´pez-Climent, M., et al., 2009. Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol. 150, 1335
1344. An, C., Mou, Z., 2011. Salicylic acid and its function in plant immunity. J. Integr. Plant Biol. 53, 412
428. Argueso, C.T., Ferreira, F.J., Kieber, J.J., 2009. Environmental perception avenues: the interaction of cytokinin and environmental response pathways. Plant Cell Environ. 32, 1147
1160. Asgher, M., Per, T.S., Masood, A., Fatma, M., Freschi, L., Corpas, F.J., et al., 2017. Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environ. Sci. Pollut. Res. 24, 2273
2285. Astier, J., Kulik, A., Koen, E., Besson-Bard, A., Bourque, S., Jeandroz, S., et al., 2012. Protein S-nitrosylation: what’s going on in plants? Free Radical Biol. Med. 53, 1101
1110. Avanci, N., Luche, D., Goldman, G., Goldman, M., 2010. Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. Genet Mol. Res. 9, 484
505. Bai, M.-Y., Shang, J.-X., Oh, E., Fan, M., Bai, Y., Zentella, R., et al., 2012. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat. Cell Biol. 14, 810. Bailey-Serres, J., Voesenek, L.A., 2010. Life in the balance: a signaling network controlling survival of flooding. Curr. Opin. Plant Biol. 13, 489
494. Bajguz, A., 2010. An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environ. Exp. Bot. 68, 175
179. Bajguz, A., Hayat, S., 2009. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol. Biochem. 47, 1
8. Balzan, S., Johal, G.S., Carraro, N., 2014. The role of auxin transporters in monocots development. Front. Plant Sci. 5, 393. Bandurska, H., Pietrowska-Borek, M., Cie´slak, M., 2012. Response of barley seedlings to water deficit and enhanced UV-B irradiation acting alone and in combination. Acta Physiol. Plant. 34, 161
171. Bannenberg, G., Martı´nez, M., Hamberg, M., Castresana, C., 2009. Diversity of the enzymatic activity in the lipoxygenase gene family of Arabidopsis thaliana. Lipids 44, 85. Basu, S., Rabara, R., 2017. Abscisic acid—an enigma in the abiotic stress tolerance of crop plants. Plant Gene 11, 90
98. Beligni, M.V., Lamattina, L., 2000. Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210, 215
221. Belkhadir, Y., Jaillais, Y., 2015. The molecular circuitry of brassinosteroid signaling. New Phytol. 206, 522
540. Bell, E., Creelman, R.A., Mullet, J.E., 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 92, 8675
8679. Benedetti, C.E., Xie, D., Turner, J.G., 1995. COI1-dependent expression of an Arabidopsis vegetative storage protein in flowers and siliques and in response to coronatine or methyl jasmonate. Plant Physiol. 109, 567
572. Benkova, E., Hejatko, J., 2009. Hormone interactions at the root apical meristem. Plant Mol. Biol. 69, 383
396. Bethke, P.C., Libourel, I.G., Jones, R.L., 2005. Nitric oxide reduces seed dormancy in Arabidopsis. J. Exp. Bot. 57, 517
526. Bishopp, A., El-Showk, S., Weijers, D., Scheres, B., Friml, J., Benkova´, E., et al., 2011. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr. Biol. 21, 917
926.

Plant Life under Changing Environment

References

445

Bonaventure, G., Schuck, S., Baldwin, I.T., 2011. Revealing complexity and specificity in the activation of lipasemediated oxylipin biosynthesis: a specific role of the Nicotiana attenuata GLA1 lipase in the activation of jasmonic acid biosynthesis in leaves and roots. Plant Cell Environ. 34, 1507
1520. Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., et al., 2005. MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone, Dev. Cell, 8. pp. 443
449. Boot, K.J., Hille, S.C., Libbenga, K.R., Peletier, L.A., van Spronsen, P.C., van Duijn, B., et al., 2016. Modelling the dynamics of polar auxin transport in inflorescence stems of Arabidopsis thaliana. J. Exp. Bot. 67, 649
666. Bray, E., 2002. Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. Plant Cell Environ. 25, 153
161. Brodersen, P., Petersen, M., Bjørn Nielsen, H., Zhu, S., Newman, M.A., Shokat, K.M., et al., 2006. Arabidopsis MAP kinase 4 regulates salicylic acid-and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J. 47, 532
546. Brodribb, T.J., McAdam, S.A., 2017. Evolution of the stomatal regulation of plant water content. Plant Physiol. 174, 639
649. pp. 00078.2017. Brugiere, N., Jiao, S., Hantke, S., Zinselmeier, C., Roessler, J.A., Niu, X., et al., 2003. Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol. 132, 1228
1240. Bu¨cker-Neto, L., Paiva, A.L.S., Machado, R.D., Arenhart, R.A., Margis-Pinheiro, M., 2017. Interactions between plant hormones and heavy metals responses. Genet. Mol. Biol. 40, 373
386. Bythell-Douglas, R., Waters, M.T., Scaffidi, A., Flematti, G.R., Smith, S.M., Bond, C.S., 2013. The structure of the karrikin-insensitive protein (KAI2) in Arabidopsis thaliana. PLoS One 8, e54758. Cai, S., Jiang, G., Ye, N., Chu, Z., Xu, X., Zhang, J., et al., 2015. A key ABA catabolic gene, OsABA8ox3, is involved in drought stress resistance in rice. PLoS One 10, e0116646. Carabelli, M., Possenti, M., Sessa, G., Ciolfi, A., Sassi, M., Morelli, G., et al., 2007. Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev. 21, 1863
1868. Cardoso, C., Zhang, Y., Jamil, M., Hepworth, J., Charnikhova, T., Dimkpa, S.O., et al., 2014. Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc. Natl. Acad. Sci. U. S.A. 111, 2379
2384. Causier, B., Ashworth, M., Guo, W., Davies, B., 2012. The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol. 158, 423
438. ˇ ´ , M., Nova´k, J., Haba´nova´, H., Cerna, H., Brzobohaty´, B., 2016. Role of the proteome in phytohormonal sigCerny naling. Biochim. Biophys. Acta (BBA)—Proteins Proteomics 1864, 1003
1015. Chai, J., Liu, J., Zhou, J., Xing, D., 2014. Mitogen-activated protein kinase 6 regulates NPR1 gene expression and activation during leaf senescence induced by salicylic acid. J. Exp. Bot. 65, 6513
6528. Chang, C., Stadler, R., 2001. Ethylene hormone receptor action in Arabidopsis. Bioessays 23, 619
627. Chang, K.N., Zhong, S., Weirauch, M.T., Hon, G., Pelizzola, M., Li, H., et al., 2013. Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. Elife 2, e00675. Chaturvedi, R., Venables, B., Petros, R.A., Nalam, V., Li, M., Wang, X., et al., 2012. An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J. 71, 161
172. Cheminant, S., Wild, M., Bouvier, F., Pelletier, S., Renou, J.-P., Erhardt, M., et al., 2011. DELLAs regulate chlorophyll and carotenoid biosynthesis to prevent photooxidative damage during seedling deetiolation in Arabidopsis. Plant Cell 23, 1849
1860. Chen, W.W., Yang, J.L., Qin, C., Jin, C.W., Mo, J.H., Ye, T., et al., 2010. Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis thaliana. Plant Physiol. 154 (2), 810
819. Chen, H., Li, Z., Xiong, L., 2012a. A plant microRNA regulates the adaptation of roots to drought stress. FEBS Lett. 586, 1742
1747. Chen, L., Song, Y., Li, S., Zhang, L., Zou, C., Yu, D., 2012b. The role of WRKY transcription factors in plant abiotic stresses. Biochim. Biophys. Acta (BBA)-Gene Regul. Mech. 1819, 120
128. Chen, Y.-A., Chi, W.-C., Trinh, N.N., Huang, L.-Y., Chen, Y.-C., Cheng, K.-T., et al., 2014. Transcriptome profiling and physiological studies reveal a major role for aromatic amino acids in mercury stress tolerance in rice seedlings. PLoS One 9, e95163.

Plant Life under Changing Environment

446

16. Phytohormonal signaling under abiotic stress

Chiang, Y., Zubo, Y., Tapken, W., Kim, H., Lavanway, A., Howard, L., et al., 2012. The GATA transcription factors GNC and CGA1 positively regulate chloroplast development, growth, and division in Arabidopsis. Plant Physiol. 160, 332
348. Chinnusamy, V., Schumaker, K., Zhu, J.K., 2004. Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J. Exp. Bot. 55, 225
236. Cho, Y.-H., Yoo, S.-D., 2015. Novel connections and gaps in ethylene signaling from the ER membrane to the nucleus. Front. Plant Sci. 5, 733. Cho, D., Kim, S.A., Murata, Y., Lee, S., Jae, S.K., Nam, H.G., et al., 2009. De-regulated expression of the plant glutamate receptor homolog AtGLR3.1 impairs long-term Ca21-programmed stomatal closure. Plant J. 58, 437
449. Choudhary, S.P., Yu, J.-Q., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.-S.P., 2012. Benefits of brassinosteroid crosstalk. Trends Plant Sci. 17, 594
605. Chung, Y., Choe, S., 2013. The regulation of brassinosteroid biosynthesis in Arabidopsis. Crit. Rev. Plant Sci. 32, 396
410. Chung, Y., Maharjan, P.M., Lee, O., Fujioka, S., Jang, S., Kim, B., et al., 2011. Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. Plant J. 66, 564
578. Claeys, H., Skirycz, A., Maleux, K., Inze´, D., 2012. DELLA signaling mediates stress-induced cell differentiation in Arabidopsis leaves through modulation of anaphase-promoting complex/cyclosome activity. Plant Physiol. 159, 739
747. Clarke, S.M., Cristescu, S.M., Miersch, O., Harren, F.J., Wasternack, C., Mur, L.A., 2009. Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol. 182, 175
187. Clouse, S.D., 2011. Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23, 1219
1230. Colebrook, E.H., Thomas, S.G., Phillips, A.L., Hedden, P., 2014. The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol. 217, 67
75. Cooper, J.W., Hu, Y., Beyyoudh, L., Dasgan, H.Y., Kunert, K., Beveridge, C.A., et al., 2018. Strigolactones positively regulate chilling tolerance in pea and in Arabidopsis. Plant Cell Environ. Available from: https://doi. org/10.1111/pce.13147. Corpas, F.J., Alche´, Jd.D., Barroso, J.B., 2013. Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front. Plant Sci. 4, 126. Crawford, N.M., 2005. Mechanisms for nitric oxide synthesis in plants. J. Exp. Bot. 57, 471
478. Creelman, R.A., Mullet, J.E., 1997. Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Biol. 48, 355
381. Danquah, A., de Zelicourt, A., Colcombet, J., Hirt, H., 2014. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv. 32, 40
52. Davie`re, J.-M., Achard, P., 2013. Gibberellin signaling in plants. Development 140, 1147
1151. Davies, W.J., Zhang, J., 1991. Root signals and the regulation of growth and development of plants in drying soil. Annu. Rev. Plant Biol. 42, 55
76. Delledonne, M., Xia, Y., Dixon, R.A., Lamb, C., 1998. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585. De Lucas, M., Daviere, J.-M., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., et al., 2008. A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480. Demkura, P.V., Abdala, G., Baldwin, I.T., Ballare´, C.L., 2010. Jasmonate-dependent and-independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense. Plant Physiol. 152, 1084
1095. De Ollas, C., Arbona, V., Go´mez-Cadenas, A., 2015. Jasmonic acid interacts with abscisic acid to regulate plant responses to water stress conditions. Plant Signal. Behav. 10, e1078953. Desikan, R., Griffiths, R., Hancock, J., Neill, S., 2002. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 99, 16314
16318. Desikan, R., Last, K., Harrett-Williams, R., Tagliavia, C., Harter, K., Hooley, R., et al., 2006. Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J. 47, 907
916. De Tullio, M.C., Jiang, K., Feldman, L.J., 2010. Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiol. Biochem. 48, 328
336.

Plant Life under Changing Environment

References

447

Dey, S., Corina Vlot, A., 2015. Ethylene responsive factors in the orchestration of stress responses in monocotyledonous plants. Front. Plant Sci. 6, 640. Dietz, K.-J., Vogel, M.O., Viehhauser, A., 2010. AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 245, 3
14. Dill, A., Thomas, S.G., Hu, J., Steber, C.M., Sun, T.P., 2004. The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16, 1392
1405. Ding, H., Zhang, A., Wang, J., Lu, R., Zhang, H., Zhang, J., et al., 2009. Identity of an ABA-activated 46 kDa mitogen-activated protein kinase from Zea mays leaves: partial purification, identification and characterization. Planta 230, 239
251. Di Rubbo, S., Irani, N.G., Russinova, E., 2011. PP2A phosphatases: the “on-off” regulatory switches of brassinosteroid signaling. Sci. Signal. 4 (172), pe25. Available from: https://doi.org/10.1126/scisignal.2002046. Divi, U.K., Krishna, P., 2009. Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. New Biotechnol. 26, 131
136. Divi, U.K., Krishna, P., 2010. Brassinosteroids confer stress tolerance. In: Plant Stress Biology: From Genomics to Systems Biology, Wiley, pp. 119
135. Divi, U.K., Rahman, T., Krishna, P., 2010. Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol. 10, 151. ˇ ˇ ´ , H., Dobrev, P., Skala´k, J., Jedelsky´, P.L., et al., 2015. The impact of heat stress tar´ , M., Storchova Dobra, J., Cerny geting on the hormonal and transcriptomic response in Arabidopsis. Plant Sci. 231, 52
61. Du, H., Liu, H., Xiong, L., 2013. Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front. Plant Sci. 4, 397. Durner, J., Klessig, D.F., 1999. Nitric oxide as a signal in plants. Curr. Opin. Plant Biol. 2, 369
374. Ecker, J.R., 1995. The ethylene signal transduction pathway in plants. Science 268, 667
675. Efroni, I., Han, S.-K., Kim, H.J., Wu, M.-F., Steiner, E., Birnbaum, K.D., et al., 2013. Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev. Cell 24, 438
445. Ellinger, D., Stingl, N., Kubigsteltig, I.I., Bals, T., Juenger, M., Pollmann, S., et al., 2010. DONGLE and DEFECTIVE IN ANTHER DEHISCENCE1 lipases are not essential for wound-and pathogen-induced jasmonate biosynthesis: redundant lipases contribute to jasmonate formation. Plant Physiol. 153, 114
127. El-Showk, S., Ruonala, R., Helariutta, Y., 2013. Crossing paths: cytokinin signalling and crosstalk. Development 140, 1373
1383. Elviri, L., Speroni, F., Careri, M., Mangia, A., di Toppi, L.S., Zottini, M., 2010. Identification of in vivo nitrosylated phytochelatins in Arabidopsis thaliana cells by liquid chromatography-direct electrospray-linear ion trap-mass spectrometry. J. Chromatogr. A 1217, 4120
4126. Epple, P., Apel, K., Bohlmann, H., 1995. An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol. 109, 813
820. Fahad, S., Hussain, S., Bano, A., Saud, S., Hassan, S., Shan, D., et al., 2015a. Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environ. Sci. Pollut. Res. 22, 4907
4921. Fahad, S., Hussain, S., Matloob, A., Khan, F.A., Khaliq, A., Saud, S., et al., 2015b. Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul. 75, 391
404. Fahad, S., Nie, L., Chen, Y., Wu, C., Xiong, D., Saud, S., et al., 2015c. Crop plant hormones and environmental stress. Sustainable Agriculture Reviews. Springer, pp. 371
400. Fancy, N.N., Bahlmann, A.K., Loake, G.J., 2017. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 40, 462
472. Farmer, E.E., Ryan, C.A., 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of woundinducible proteinase inhibitors. Plant Cell 4, 129
134. Farnese, F.S., de Oliveira, J.A., Gusman, G.S., Lea˜o, G.A., Ribeiro, C., Siman, L.I., et al., 2013. Plant responses to arsenic: the role of nitric oxide. Water Air Soil Pollut. 224, 1660. Fediuc, E., Lips, S.H., Erdei, L., 2005. O-acetylserine (thiol) lyase activity in Phragmites and Typha plants under cadmium and NaCl stress conditions and the involvement of ABA in the stress response. J. Plant Physiol. 162, 865
872.

Plant Life under Changing Environment

448

16. Phytohormonal signaling under abiotic stress

Feng, S., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J., Wang, F., et al., 2008. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475
479. Feng, J., Wang, C., Chen, Q., Chen, H., Ren, B., Li, X., et al., 2013. S-Nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nat. Commun. 4, 1529. Feurtado, J.A., Huang, D., Wicki-Stordeur, L., Hemstock, L.E., Potentier, M.S., Tsang, E.W., et al., 2011. The Arabidopsis C2H2 zinc finger INDETERMINATE DOMAIN1/ENHYDROUS promotes the transition to germination by regulating light and hormonal signaling during seed maturation. Plant Cell 23, 1772
1794. Finkelstein, R., 2013. Abscisic acid synthesis and response, Arabidopsis Book, 11. p. e0166. Finkelstein, R.R., Gampala, S.S., Rock, C.D., 2002. Abscisic acid signaling in seeds and seedlings. Plant Cell 14, S15
S45. Flematti, G.R., Waters, M.T., Scaffidi, A., Merritt, D.J., Ghisalberti, E.L., Dixon, K.W., et al., 2013. Karrikin and cyanohydrin smoke signals provide clues to new endogenous plant signaling compounds. Mol. Plant 6, 29
37. Fraire-Vela´zquez, S., Rodrı´guez-Guerra, R., Sa´nchez-Caldero´n, L., 2011. Abiotic and biotic stress response crosstalk in plants. Abiotic Stress Response in Plants-Physiological, Biochemical and Genetic Perspectives. InTech. Fre´bort, I., Kowalska, M., Hluska, T., Fre´bortova´, J., Galuszka, P., 2011. Evolution of cytokinin biosynthesis and degradation. J. Exp. Bot. 62, 2431
2452. Freschi, L., 2013. Nitric oxide and phytohormone interactions: current status and perspectives. Front. Plant Sci. 4, 398. Fu, Z.Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., et al., 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228
232. Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., et al., 2009. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50, 2123
2132. Fujita, Y., Yoshida, T., Yamaguchi-Shinozaki, K., 2013. Pivotal role of the AREB/ABF-SnRK2 pathway in ABREmediated transcription in response to osmotic stress in plants. Physiol. Plant. 147, 15
27. Fukao, T., Yeung, E., Bailey-Serres, J., 2011. The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23, 412
427. Furihata, T., Maruyama, K., Fujita, Y., Umezawa, T., Yoshida, R., Shinozaki, K., et al., 2006. Abscisic aciddependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc. Natl. Acad. Sci. U.S.A. 103, 1988
1993. Gagne, J.M., Smalle, J., Gingerich, D.J., Walker, J.M., Yoo, S.-D., Yanagisawa, S., et al., 2004. Arabidopsis EIN3binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc. Natl. Acad. Sci. U.S.A. 101, 6803
6808. Gallego-Bartolome´, J., Minguet, E.G., Marı´n, J.A., Prat, S., Bla´zquez, M.A., Alabadı´, D., 2010. Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Mol. Biol. Evol. 27, 1247
1256. Gallego-Bartolome´, J., Alabadı´, D., Bla´zquez, M.A., 2011. DELLA-induced early transcriptional changes during etiolated development in Arabidopsis thaliana. PLoS One 6, e23918. Gallego-Bartolome´, J., Minguet, E.G., Grau-Enguix, F., Abbas, M., Locascio, A., Thomas, S.G., et al., 2012. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 13446
13451. Galuszka, P., Popelkova´, H., Werner, T., Fre´bortova´, J., Pospı´sˇ ilova´, H., Mik, V., et al., 2007. Biochemical characterization of cytokinin oxidases/dehydrogenases from Arabidopsis thaliana expressed in Nicotiana tabacum L. J. Plant Growth Regul. 26, 255
267. Gamalero, E., Glick, B.R., 2012. Ethylene and abiotic stress tolerance in plants. In: Ahmed, P., Prasad, M.N.V. (Eds.), Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Springer, New York, pp. 395
412. Gao, Y., Zhao, Y., 2014. Auxin biosynthesis and catabolism. In: Zaˇz´ımalova´, et al., (Eds.), Auxin and Its Role in Plant Development. Springer-Verlag, Wien. Garcia-Mata, C., Lamattina, L., 2002. Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 128, 790
792. Garcia-Mata, C., Lamattina, L., 2007. Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium-and nitric oxide-mediated signaling pathways. Nitric Oxide 17, 143
151.

Plant Life under Changing Environment

References

449

Ghanem, M.E., Albacete, A., Smigocki, A.C., Fre´bort, I., Pospı´sˇ ilova´, H., Martı´nez-Andu´jar, C., et al., 2010. Rootsynthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. J. Exp. Bot. 62, 125
140. Glauser, G., Dubugnon, L., Mousavi, S.A., Rudaz, S., Wolfender, J.-L., Farmer, E.E., 2009. Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J. Biol. Chem. 284, 34506
34513. Gordon, S.P., Chickarmane, V.S., Ohno, C., Meyerowitz, E.M., 2009. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. U.S.A. 106, 16529
16534. Gou, X., Yin, H., He, K., Du, J., Yi, J., Xu, S., et al., 2012. Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet. 8, e1002452. Grant, J.J., Loake, G.J., 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124, 21
30. Griffiths, J., Murase, K., Rieu, I., Zentella, R., Zhang, Z.-L., Powers, S.J., et al., 2006. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18, 3399
3414. Gru¨n, S., Lindermayr, C., Sell, S., Durner, J., 2006. Nitric oxide and gene regulation in plants. J. Exp. Bot. 57, 507
516. Gruszka, D., 2013. The brassinosteroid signaling pathway—new key players and interconnections with other signaling networks crucial for plant development and stress tolerance. Int. J. Mol. Sci. 14, 8740
8774. Gudesblat, G.E., Russinova, E., 2011. Plants grow on brassinosteroids. Curr. Opin. Plant Biol. 14, 530
537. Guo, H., Ecker, J.R., 2003. Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115, 667
677. Guo, F.-Q., Crawford, N.M., 2005. Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17, 3436
3450. Gupta, S., Rashotte, A.M., 2012. Down-stream components of cytokinin signaling and the role of cytokinin throughout the plant. Plant Cell Rep. 31, 801
812. Gupta, K.J., Fernie, A.R., Kaiser, W.M., van Dongen, J.T., 2011. On the origins of nitric oxide. Trends Plant Sci. 16, 160
168. Ha, S., Vankova, R., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.-S.P., 2012. Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci. 17, 172
179. Ha, C.V., Leyva-Gonza´lez, M.A., Osakabe, Y., Tran, U.T., Nishiyama, R., Watanabe, Y., et al., 2014. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc. Natl. Acad. Sci. U.S.A. 111, 851
856. Hahn, A., Harter, K., 2009. Mitogen-activated protein kinase cascades and ethylene: signaling, biosynthesis, or both? Plant Physiol. 149, 1207
1210. Hamdoun, S., Liu, Z., Gill, M., Yao, N., Lu, H., 2013. Dynamics of defense responses and cell fate change during Arabidopsis-Pseudomonas syringae interactions. PLoS One 8, e83219. Hao, J., Yin, Y., Fei, S.-z, 2013. Brassinosteroid signaling network: implications on yield and stress tolerance. Plant Cell Rep. 32, 1017
1030. Harrison, M.A., 2012. Cross-talk between phytohormone signaling pathways under both optimal and stressful environmental conditions. Phytohormones and Abiotic Stress Tolerance in Plants. Springer, pp. 49
76. Hasanuzzaman, M., Fujita, M., 2013. Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22, 584
596. Haubrick, L.L., Torsethaugen, G., Assmann, S.M., 2006. Effect of brassinolide, alone and in concert with abscisic acid, on control of stomatal aperture and potassium currents of Vicia faba guard cell protoplasts. Physiol. Plant. 128, 134
143. Hause, B., Maier, W., Miersch, O., Kramell, R., Strack, D., 2002. Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol. 130, 1213
1220. Hauvermale, A.L., Ariizumi, T., Steber, C.M., 2012. Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol. 160, 83
92. Hayat, Q., Hayat, S., Irfan, M., Ahmad, A., 2010. Effect of exogenous salicylic acid under changing environment: a review. Environ. Exp. Bot. 68, 14
25.

Plant Life under Changing Environment

450

16. Phytohormonal signaling under abiotic stress

Hayat, S., Maheshwari, P., Wani, A.S., Irfan, M., Alyemeni, M.N., Ahmad, A., 2012. Comparative effect of 28 homobrassinolide and salicylic acid in the amelioration of NaCl stress in Brassica juncea L. Plant Physiol. Biochem. 53, 61
68. Hedden, P., Thomas, S.G., 2012. Gibberellin biosynthesis and its regulation. Biochem. J. 444, 11
25. Herbette, S., Taconnat, L., Hugouvieux, V., Piette, L., Magniette, M.-L., Cuine, S., et al., 2006. Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88, 1751
1765. Herrera-Va´squez, A., Salinas, P., Holuigue, L., 2015. Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front. Plant Sci. 6, 171. Hirano, K., Kouketu, E., Katoh, H., Aya, K., Ueguchi-Tanaka, M., Matsuoka, M., 2012. The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity. Plant J. 71, 443
453. Holbrook, N.M., Shashidhar, V., James, R.A., Munns, R., 2002. Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. J. Exp. Bot. 53, 1503
1514. Hong, G.-J., Xue, X.-Y., Mao, Y.-B., Wang, L.-J., Chen, X.-Y., 2012. Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24, 2635
2648. Horva´th, E., Szalai, G., Janda, T., 2007. Induction of abiotic stress tolerance by salicylic acid signaling. J. Plant Growth Regul. 26, 290
300. Hossain, M.A., Munemasa, S., Uraji, M., Nakamura, Y., Mori, I.C., Murata, Y., 2011. Involvement of endogenous abscisic acid in methyl jasmonate-induced stomatal closure in Arabidopsis. Plant Physiol. 156, 430
438. Hou, X., Lee, L.Y.C., Xia, K., Yan, Y., Yu, H., 2010. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev. Cell 19, 884
894. Hu, X., Neill, S.J., Tang, Z., Cai, W., 2005a. Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol. 137, 663
670. Hu, Y., Jia, W., Wang, J., Zhang, Y., Yang, L., Lin, Z., 2005b. Transgenic tall fescue containing the Agrobacterium tumefaciens ipt gene shows enhanced cold tolerance. Plant Cell Rep. 23, 705
709. Huang, Y., Li, H., Hutchison, C.E., Laskey, J., Kieber, J.J., 2003. Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J. 33, 221
233. Huang, D., Wu, W., Abrams, S.R., Cutler, A.J., 2008. The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J. Exp. Bot. 59, 2991
3007. Huang, J.G., Yang, M., Liu, P., Yang, G.D., Wu, C.A., Zheng, C.C., 2009. GhDREB1 enhances abiotic stress tolerance, delays GA-mediated development and represses cytokinin signalling in transgenic Arabidopsis. Plant Cell Environ. 32, 1132
1145. Huang, G.-T., Ma, S.-L., Bai, L.-P., Zhang, L., Ma, H., Jia, P., et al., 2012. Signal transduction during cold, salt, and drought stresses in plants. Mol. Biol. Rep. 39, 969
987. Hubbard, K.E., Nishimura, N., Hitomi, K., Getzoff, E.D., Schroeder, J.I., 2010. Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev. 24, 1695
1708. Hwang, I., Sheen, J., Mu¨ller, B., 2012. Cytokinin signaling networks. Annu. Rev. Plant Biol. 63, 353
380. Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T., Shinozaki, K., 2000. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 24, 655
665. Iglesias, M.J., Terrile, M.C., Bartoli, C.G., D’Ippo´lito, S., Casalongue´, C.A., 2010. Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol. Biol. 74, 215
222. Iqbal, N., Umar, S., Khan, N.A., Khan, M.I.R., 2014. A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ. Exp. Bot. 100, 34
42. Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I., Okada, K., 2001. The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13, 2191
2209. Ito, T., Ng, K.-H., Lim, T.-S., Yu, H., Meyerowitz, E.M., 2007. The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 19, 3516
3529. Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., et al., 2001. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J. 27, 325
333. Jaillais, Y., Belkhadir, Y., Balsema˜o-Pires, E., Dangl, J.L., Chory, J., 2011. Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation. Proc. Natl. Acad. Sci. U.S.A. 108, 8503
8507.

Plant Life under Changing Environment

References

451

Jamil, M., Charnikhova, T., Cardoso, C., Jamil, T., Ueno, K., Verstappen, F., et al., 2011. Quantification of the relationship between strigolactones and Striga hermonthica infection in rice under varying levels of nitrogen and phosphorus. Weed Res. 51, 373
385. Janda, M., Ruelland, E., 2015. Magical mystery tour: salicylic acid signalling. Environ. Exp. Bot. 114, 117
128. Jeon, J., Kim, J., 2013. Arabidopsis response regulator1 and Arabidopsis histidine phosphotransfer protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant Physiol. 161, 408
424. Jeon, J., Kim, N.Y., Kim, S., Kang, N.Y., Nova´k, O., Ku, S.-J., et al., 2010. A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J. Biol. Chem. 285, 23371
23386. Jeong, J.S., Kim, Y.S., Baek, K.H., Jung, H., Ha, S.-H., Do Choi, Y., et al., 2010. Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol. 153, 185
197. Jiang, Y.P., Cheng, F., Zhou, Y.H., Xia, X.J., Mao, W.H., Shi, K., et al., 2012a. Cellular glutathione redox homeostasis plays an important role in the brassinosteroid-induced increase in CO2 assimilation in Cucumis sativus. New Phytol. 194, 932
943. Jiang, Y.P., Cheng, F., Zhou, Y.H., Xia, X.J., Mao, W.H., Shi, K., et al., 2012b. Brassinosteroid-induced CO2 assimilation is associated with increased stability of redox-sensitive photosynthetic enzymes in the chloroplasts in cucumber plants. Biochem. Biophys. Res. Commun. 426, 390
394. Jiang, L., Liu, X., Xiong, G., Liu, H., Chen, F., Wang, L., et al., 2013. DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504, 401. Jiang, Z., Li, J., Qu, L.-J., 2017. Auxins. In: Li, J., Li, C., Smith, S. (Eds.), Hormone Metabolism and Signaling in Plants. Elsevier Ltd. Joshi, M.S., Ponthier, J.L., Lancaster Jr., J.R., 1999. Cellular antioxidant and pro-oxidant actions of nitric oxide. Free Radical Biol. Med. 27, 1357
1366. Joshi, R., Wani, S.H., Singh, B., Bohra, A., Dar, Z.A., Lone, A.A., et al., 2016. Transcription factors and plants response to drought stress: current understanding and future directions. Front. Plant Sci. 7, 1029. Joshi, R., Singla-Pareek, S.L., Pareek, A., 2018. Engineering abiotic stress response in plants for biomass production. J. Biol. Chem. 293, 5035
5043. jbc. TM117. 000232. Joudoi, T., Shichiri, Y., Kamizono, N., Akaike, T., Sawa, T., Yoshitake, J., et al., 2013. Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis. Plant Cell 25, 558
571. Ju, C., Chang, C., 2012. Advances in ethylene signalling: protein complexes at the endoplasmic reticulum membrane. AoB Plants 2012, pls031. Available from: https://doi.org/10.1093/aobpla/pls031. Ju, C., Yoon, G.M., Shemansky, J.M., Lin, D.Y., Ying, Z.I., Chang, J., et al., 2012. CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 19486
19491. Jumali, S.S., Said, I.M., Ismail, I., Zainal, Z., 2011. Genes induced by high concentration of salicylic acid in ‘Mitragyna speciosa’. Aust. J. Crop Sci. 5, 296. Jung, H.W., Tschaplinski, T.J., Wang, L., Glazebrook, J., Greenberg, J.T., 2009. Priming in systemic plant immunity. Science 324, 89
91. Kagale, S., Divi, U.K., Krochko, J.E., Keller, W.A., Krishna, P., 2007. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225, 353
364. Kaneko, M., Itoh, H., Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Ashikari, M., et al., 2003. Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J. 35, 104
115. Kang, N.Y., Cho, C., Kim, N.Y., Kim, J., 2012. Cytokinin receptor-dependent and receptor-independent pathways in the dehydration response of Arabidopsis thaliana. J. Plant Physiol. 169, 1382
1391. Kanyuka, K., Praekelt, U., Franklin, K.A., Billingham, O.E., Hooley, R., Whitelam, G.C., et al., 2003. Mutations in the huge Arabidopsis gene BIG affect a range of hormone and light responses. Plant J. 35, 57
70. Kende, H., 1989. Enzymes of ethylene biosynthesis. Plant Physiol. 91, 1
4. Keunen, E., Schellingen, K., Vangronsveld, J., Cuypers, A., 2016. Ethylene and metal stress: small molecule, big impact. Front. Plant Sci. 7, 23. Khan, M.I.R., Khan, N.A., 2013. Salicylic acid and jasmonates: approaches in abiotic stress tolerance. J. Plant Biochem. Physiol. 1, e113.

Plant Life under Changing Environment

452

16. Phytohormonal signaling under abiotic stress

Khan, M., Iqbal, N., Masood, A., Khan, N., 2012b. Variation in salt tolerance of wheat cultivars: role of glycinebetaine and ethylene. Pedosphere 22, 746
754. Khan, N.A., Nazar, R., Iqbal, N., Anjum, N.A., 2012c. Phytohormones and Abiotic Stress Tolerance in Plants. Springer Science & Business Media. Khan, M.I.R., Fatma, M., Per, T.S., Anjum, N.A., Khan, N.A., 2015. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front. Plant Sci. 6, 462. Khripach, V., Zhabinskii, V., de Groot, A., 2000. Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI century. Ann. Bot. 86, 441
447. Kieber, J.J., Schaller, G.E., 2014. Cytokinins, Arabidopsis Book, 12. p. e0168. Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A., Ecker, J.R., 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72, 427
441. Kim, S., Kang, Jy, Cho, D.I., Park, J.H., Kim, S.Y., 2004. ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J. 40, 75
87. Kim, T.-H., Bo¨hmer, M., Hu, H., Nishimura, N., Schroeder, J.I., 2010. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca21 signaling. Annu. Rev. Plant Biol. 61, 561
591. Kim, J.-S., Mizoi, J., Yoshida, T., Fujita, Y., Nakajima, J., Ohori, T., et al., 2011a. An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol. 52, 2136
2146. Kim, T.-W., Guan, S., Burlingame, A.L., Wang, Z.-Y., 2011b. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell 43, 561
571. Kim, J.-S., Mizoi, J., Kidokoro, S., Maruyama, K., Nakajima, J., Nakashima, K., et al., 2012. Arabidopsis growthregulating factor7 functions as a transcriptional repressor of abscisic acid- and osmotic stress-responsive genes, including DREB2A. Plant Cell 24, 3393
3405. Kim, Y.-H., Khan, A.L., Kim, D.-H., Lee, S.-Y., Kim, K.-M., Waqas, M., et al., 2014. Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones. BMC Plant Biol. 14, 13. Knight, H., Knight, M.R., 2001. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci. 6, 262
267. Koh, S., Lee, S.-C., Kim, M.-K., Koh, J.H., Lee, S., An, G., et al., 2007. T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol. Biol. 65, 453
466. Kohli, A., Sreenivasulu, N., Lakshmanan, P., Kumar, P.P., 2013. The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stresses. Plant cell Rep. 32, 945
957. Koltai, H., Kapulnik, Y., 2014. Strigolactones involvement in root development and communications. Root Engineering. Springer, pp. 203
219. Kong, J., Dong, Y., Xu, L., Liu, S., Bai, X., 2014. Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L. Bot. Stud. 55, 9. Konishi, M., Yanagisawa, S., 2008. Ethylene signaling in Arabidopsis involves feedback regulation via the elaborate control of EBF2 expression by EIN3. Plant J. 55, 821
831. Korasick, D.A., Enders, T.A., Strader, L.C., 2013. Auxin biosynthesis and storage forms. J. Exp. Bot. 64, 2541
2555. Kovacs, I., Lindermayr, C., 2013. Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation. Front. Plant Sci. 4, 137. Krishna, P., 2003. Brassinosteroid-mediated stress responses. J. Plant Growth Regul. 22, 289
297. Kumar, M.N., Jane, W.-N., Verslues, P.E., 2013. Role of the putative osmosensor Arabidopsis Histidine Kinase1 in dehydration avoidance and low-water-potential response. Plant Physiol. 161, 942
953. Kundu, S., Gantait, S., 2017. Abscisic acid signal crosstalk during abiotic stress response. Plant Gene 11, 61
69. Kwak, J.M., Mori, I.C., Pei, Z.M., Leonhardt, N., Torres, M.A., Dangl, J.L., et al., 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623
2633. Lee, S.C., Lim, C.W., Lan, W., He, K., Luan, S., 2013. ABA signaling in guard cells entails a dynamic protein
protein interaction relay from the PYL-RCAR family receptors to ion channels. Mol. Plant 6, 528
538.

Plant Life under Changing Environment

References

453

Leterrier, M., Chaki, M., Airaki, M., Valderrama, R., Palma, J.M., Barroso, J.B., et al., 2011. Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signal. Behav. 6, 789
793. Li, J., 2010. Regulation of the nuclear activities of brassinosteroid signaling. Curr. Opin. Plant Biol. 13, 540
547. Li, W., Tran, L.S., 2015. Are karrikins involved in plant abiotic stress responses? Trends Plant Sci. 20, 535
538. Li, L., Ye, H., Guo, H., Yin, Y., 2010. Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc. Natl. Acad. Sci. U.S.A. 107, 3918
3923. Li, Q.-F., Wang, C., Jiang, L., Li, S., Sun, S.S., He, J.-X., 2012a. An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci. Signal 5, ra72. Available from: https://doi.org/10.1126/scisignal.2002908. Li, Z.-Y., Xu, Z.-S., He, G.-Y., Yang, G.-X., Chen, M., Li, L.-C., et al., 2012b. A mutation in Arabidopsis BSK5 encoding a brassinosteroid-signaling kinase protein affects responses to salinity and abscisic acid. Biochem. Biophys. Res. Commun. 426, 522
527. Liu, X., Huang, B., 2002. Cytokinin effects on creeping bentgrass response to heat stress. Crop Sci. 42, 466
472. Liu, J., Blaylock, L.A., Endre, G., Cho, J., Town, C.D., VandenBosch, K.A., et al., 2003. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15, 2106
2123. Liu, J., He, H., Vitali, M., Visentin, I., Charnikhova, T., Haider, I., et al., 2015. Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta 241, 1435
1451. Liu, H., Carvalhais, L.C., Kazan, K., Schenk, P.M., 2016. Development of marker genes for jasmonic acid signaling in shoots and roots of wheat. Plant Signal. Behav. 11, e1176654. Liu, J., Zhang, D., Sun, X., Ding, T., Lei, B., Zhang, C., 2017. Structure-activity relationship of brassinosteroids and their agricultural practical usages. Steroids 124, 1
17. Locato, V., Paradiso, A., Sabetta, W., De Gara, L., de Pinto, M.C., 2016. Chapter nine
Nitric oxide and reactive oxygen species in PCD signaling. Adv. Bot. Res. 77, 165
192. Lo´pez-Ra´ez, J.A., Kohlen, W., Charnikhova, T., Mulder, P., Undas, A.K., Sergeant, M.J., et al., 2010. Does abscisic acid affect strigolactone biosynthesis? New Phytol. 187, 343
354. Lu, M., Zhang, Y., Tang, S., Pan, J., Yu, Y., Han, J., et al., 2016. AtCNGC2 is involved in jasmonic acid-induced calcium mobilization. J. Exp. Bot. 67, 809
819. Ludwig-Mu¨ller, J., 2011. Auxin conjugates: their role for plant development and in the evolution of land plants. J. Exp. Bot. 62, 1757
1773. Luo, X., Bai, X., Sun, X., Zhu, D., Liu, B., Ji, W., et al., 2013. Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. J. Exp. Bot. 64, 2155
2169. Magome, H., Yamaguchi, S., Hanada, A., Kamiya, Y., Oda, K., 2008. The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J. 56, 613
626. Ma¨ho¨nen, A.P., Bonke, M., Kauppinen, L., Riikonen, M., Benfey, P.N., Helariutta, Y., 2000. A novel twocomponent hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 14, 2938
2943. Maksymiec, W., 2007. Signaling responses in plants to heavy metal stress. Acta Physiol. Plant. 29, 177. Maksymiec, W., Wianowska, D., Dawidowicz, A.L., Radkiewicz, S., Mardarowicz, M., Krupa, Z., 2005. The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J. Plant Physiol. 162, 1338
1346. Maksymiec, W., Wojcik, M., Krupa, Z., 2007. Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere 66, 421
427. Mano, Y., Nemoto, K., 2012. The pathway of auxin biosynthesis in plants. J. Exp. Bot. 63, 2853
2872. Marakli, S., Gozukirmizi, N., 2016. Abiotic stress alleviation with brassinosteroids in plant roots. Abiotic and Biotic Stress in Plants-Recent Advances and Future Perspectives. InTech. Martins, S., Montiel-Jorda, A., Cayrel, A., Huguet, S., Paysant-Le Roux, C., Ljung, K., et al., 2017. Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature. Nat. Commun. 8, 309.

Plant Life under Changing Environment

454

16. Phytohormonal signaling under abiotic stress

Marzec, M., 2016. Perception and signaling of strigolactones. Front. Plant Sci. 7, 1260. Marzec, M., Muszynska, A., Gruszka, D., 2013. The role of strigolactones in nutrient-stress responses in plants. Int. J. Mol. Sci. 14, 9286
9304. Mason, M.G., Jha, D., Salt, D.E., Tester, M., Hill, K., Kieber, J.J., et al., 2010. Type-B response regulators ARR1 and ARR12 regulate expression of AtHKT1; 1 and accumulation of sodium in Arabidopsis shoots. Plant J. 64, 753
763. Mata-Pe´rez, C., Sa´nchez-Calvo, B., Padilla, M.N., Begara-Morales, J.C., Luque, F., Melguizo, M., et al., 2016. Nitrofatty acids in plant signaling: nitro-linolenic acid induces the molecular chaperone network in Arabidopsis. Plant Physiol. 170, 686
701. Mayer, B., Hemmens, B., 1997. Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem. Sci. 22, 477
481. Mayzlish-Gati, E., De-Cuyper, C., Goormachtig, S., Beeckman, T., Vuylsteke, M., Brewer, P.B., et al., 2012. Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol. 160, 1329
1341. McAdam, S.A., Manzi, M., Ross, J.J., Brodribb, T.J., Go´mez-Cadenas, A., 2016. Uprooting an abscisic acid paradigm: shoots are the primary source. Plant Signal. Behav. 11, 652
659. Mishra, S., Upadhyay, S., Shukla, R.K., 2017. The role of strigolactones and their potential cross-talk under hostile ecological conditions in plants. Front. Physiol. 7, 691. Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405
410. Miyawaki, K., Tarkowski, P., Matsumoto-Kitano, M., Kato, T., Sato, S., Tarkowska, D., et al., 2006. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 103, 16598
16603. Mizoguchi, M., Umezawa, T., Nakashima, K., Kidokoro, S., Takasaki, H., Fujita, Y., et al., 2010. Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression. Plant Cell Physiol. 51, 842
847. Montero-Palmero, M.B., Martı´n-Barranco, A., Escobar, C., Herna´ndez, L.E., 2014. Early transcriptional responses to mercury: a role for ethylene in mercury-induced stress. New Phytol. 201, 116
130. Munne´-Bosch, S., Mu¨ller, M., 2013. Hormonal cross-talk in plant development and stress responses. Front. Plant Sci. 4, 529. Murase, K., Hirano, Y., Sun, T.-p, Hakoshima, T., 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456, 459. Nakamura, A., Higuchi, K., Goda, H., Fujiwara, M.T., Sawa, S., Koshiba, T., et al., 2003. Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol. 133, 1843
1853. Nakamura, H., Xue, Y.-L., Miyakawa, T., Hou, F., Qin, H.-M., Fukui, K., et al., 2013. Molecular mechanism of strigolactone perception by DWARF14. Nat. Commun. 4, 2613. Nakamura, A., Tochio, N., Fujioka, S., Ito, S., Kigawa, T., Shimada, Y., et al., 2017. Molecular actions of two synthetic brassinosteroids, iso-carbaBL and 6-deoxoBL, which cause altered physiological activities between Arabidopsis and rice. PLoS One 12, e0174015. Nakano, T., Suzuki, K., Fujimura, T., Shinshi, H., 2006. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140, 411
432. Nakashima, K., Shinwari, Z.K., Sakuma, Y., Seki, M., Miura, S., Shinozaki, K., et al., 2000. Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration-and high-salinity-responsive gene expression. Plant Mol. Biol. 42, 657
665. Nam, K.H., Li, J., 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203
212. Nambara, E., Marion-Poll, A., 2005. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 56, 165
185. Nazar, R., Umar, S., Khan, N.A., 2015. Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal. Behav. 10, e1003751. Neill, S., Desikan, R., Hancock, J., 2002. Hydrogen peroxide signalling. Curr. Opin. Plant Biol. 5, 388
395. Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J., et al., 2008. Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot. 59, 165
176.

Plant Life under Changing Environment

References

455

Nguyen, D., Rieu, I., Mariani, C., van Dam, N.M., 2016. How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Mol. Biol. 91, 727
740. Ni, W., Xu, S.L., Chalkley, R.J., Pham, T.N.D., Guan, S., Maltby, D.A., et al., 2013. Multisite light-induced phosphorylation of the transcription factor PIF3 is necessary for both its rapid degradation and concomitant negative feedback modulation of photoreceptor phyB levels in Arabidopsis. Plant Cell 25, 2679
2698. Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N., Ohashi, Y., 1998. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39, 500
507. Nishiyama, R., Watanabe, Y., Fujita, Y., Le, D.T., Kojima, M., Werner, T., et al., 2011. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23, 2169
2183. Nishiyama, R., Watanabe, Y., Leyva-Gonzalez, M.A., et al., 2013. Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc. Natl. Acad. Sci. U.S.A. 110, 4840
4845. Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Tax, F.E., Yoshida, S., et al., 2000. Biosynthetic pathways of brassinolide in Arabidopsis. Plant Physiol. 124, 201
210. Normanly, J., 2010. Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harbor Perspect. Biol. 2, a001594. O’Brien, J.A., Benkova´, E., 2013. Cytokinin cross-talking during biotic and abiotic stress responses. Front. Plant Sci. 4, 451. Ogawa, M., Hanada, A., Yamauchi, Y., Kuwahara, A., Kamiya, Y., Yamaguchi, S., 2003. Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15 (7), 1591
1604. O’Neill, D.P., Davidson, S.E., Clarke, V.C., Yamauchi, Y., Yamaguchi, S., Kamiya, Y., et al., 2010. Regulation of the gibberellin pathway by auxin and DELLA proteins. Planta 232, 1141
1149. Oh, S.-J., Kim, Y.S., Kwon, C.-W., Park, H.K., Jeong, J.S., Kim, J.-K., 2009. Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol. 150, 1368
1379. Oh, E., Zhu, J.-Y., Wang, Z.-Y., 2012. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802. Pagnussat, G.C., Simontacchi, M., Puntarulo, S., Lamattina, L., 2002. Nitric oxide is required for root organogenesis. Plant Physiol. 129, 954
956. Pan, J., Zhang, M., Kong, X., Xing, X., Liu, Y., Zhou, Y., et al., 2012. ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta 235, 661
676. Pandey, A., Sharma, M., Pandey, G.K., 2016. Emerging roles of strigolactones in plant responses to stress and development. Front. Plant Sci. 7, 434. Pantin, F., Monnet, F., Jannaud, D., Costa, J.M., Renaud, J., Muller, B., et al., 2013. The dual effect of abscisic acid on stomata. New Phytol. 197, 65
72. Pareek, A., Sopory, S.K., Bohnert, H., 2009. Abiotic Stress Adaptation in Plants. Springer. Park, S.W., Kaimoyo, E., Kumar, D., Mosher, S., Klessig, D.F., 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113
116. Park, H.-Y., Seok, H.-Y., Park, B.-K., Kim, S.-H., Goh, C.-H., Lee, B.-H., et al., 2008. Overexpression of Arabidopsis ZEP enhances tolerance to osmotic stress. Biochem. Biophys. Res. Commun. 375, 80
85. Park, S.-Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H., Zhao, Y., et al., 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068
1071. Pauwels, L., Inze´, D., Goossens, A., 2009. Jasmonate-inducible gene: what does it mean? Trends Plant Sci. 14, 87
91. Pedroso, M., Durzan, D., 2000. Effect of different gravity environments on DNA fragmentation and cell death in Kalanchoe leaves. Ann. Bot. 86, 983
994. Pei, Z.-M., Murata, Y., Benning, G., Thomine, S., Klu¨sener, B., Allen, G.J., et al., 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731. Peleg, Z., Blumwald, E., 2011. Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 14, 290
295. Peleg, Z., Reguera, M., Tumimbang, E., Walia, H., Blumwald, E., 2011. Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol. J. 9, 747
758.

Plant Life under Changing Environment

456

16. Phytohormonal signaling under abiotic stress

Penninckx, I.A., Thomma, B.P., Buchala, A., Me´traux, J.-P., Broekaert, W.F., 1998. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10, 2103
2113. Per, T.S., Khan, M.I.R., Anjum, N.A., Masood, A., Hussain, S.J., Khan, N.A., 2018. Jasmonates in plants under abiotic stresses: crosstalk with other phytohormones matters. Environ. Exp. Bot. 145, 104
120. Pe´ret, B., Desnos, T., Jost, R., Kanno, S., Berkowitz, O., Nussaume, L., 2014. Root architecture responses: in search of phosphate. Plant Physiol. 166, 1713
1723. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., et al., 2000. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111
1120. Poschenrieder, C., Gunse, B., Barcelo, J., 1989. Influence of cadmium on water relations, stomatal resistance, and abscisic acid content in expanding bean leaves. Plant Physiol. 90, 1365
1371. Pospisilova, J., Batkova, P., 2004. Effects of pre-treatments with abscisic acid and/or benzyladenine on gas exchange of French bean, sugar beet, and maize leaves during water stress and after rehydration. Biol. Plant. 48, 395
399. Pospisilova, J., Vagner, M., Malbeck, J., Travnickova, A., Batkova, P., 2005. Interactions between abscisic acid and cytokinins during water stress and subsequent rehydration. Biol. Plant. 49, 533
540. Potuschak, T., Lechner, E., Parmentier, Y., Yanagisawa, S., Grava, S., Koncz, C., et al., 2003. EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115, 679
689. Powers, S.K., Strader, L.C., 2016. Up in the air: untethered factors of auxin response. F1000Research 5, 133. Prandi, C., Cardinale, F., 2014. Strigolactones: a new class of plant hormones with multifaceted roles. eLS. John Wiley & Sons Ltd, Chichester. Qiao, H., Chang, K.N., Yazaki, J., Ecker, J.R., 2009. Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev. 23, 512
521. Qiao, H., Shen, Z., Huang, S.-sC., Schmitz, R.J., Urich, M.A., Briggs, S.P., et al., 2012. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338, 390
393. 1224344. Qin, X., Zeevaart, J.A., 1999. The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc. Natl. Acad. Sci. U.S.A. 96, 15354
15361. Qin, F., Sakuma, Y., Tran, L.-S.P., Maruyama, K., Kidokoro, S., Fujita, Y., et al., 2008. Arabidopsis DREB2Ainteracting proteins function as RING E3 ligases and negatively regulate plant drought stress
responsive gene expression. Plant Cell 20, 1693
1707. Qin, F., Kodaira, K.-S., Maruyama, K., Mizoi, J., Tran, L.-S.P., Fujita, Y., et al., 2011a. SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol. 157, 1900
1913. Qin, F., Shinozaki, K., Yamaguchi-Shinozaki, K., 2011b. Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol. 52, 1569
1582. Qiu, L., Xie, F., Yu, J., Wen, C.-K., 2012. Arabidopsis RTE1 is essential to ethylene receptor ETR1 amino-terminal signaling independent of CTR1. Plant Physiol. 159, 1263
1276. Qu, T., Liu, R., Wang, W., An, L., Chen, T., Liu, G., et al., 2011. Brassinosteroids regulate pectin methylesterase activity and AtPME41 expression in Arabidopsis under chilling stress. Cryobiology 63, 111
117. Raja, V., Majeed, U., Kang, H., Andrabi, K.I., John, R., 2017. Abiotic stress: interplay between ROS, hormones and MAPKs. Environ. Exp. Bot. 137, 142
157. Rajewska, I., Talarek, M., Bajguz, A., 2016. Brassinosteroids and response of plants to heavy metals action. Front. Plant Sci. 7, 629. Rao, X., Dixon, R.A., 2017. Brassinosteroid mediated cell wall remodeling in grasses under abiotic stress. Front. Plant Sci. 8, 806. Rejeb, I.B., Pastor, V., Mauch-Mani, B., 2014. Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 3, 458
475. Ribeiro, D.M., Desikan, R., Bright, J., Confraria, A., Harrison, J., Hancock, J.T., et al., 2009. Differential requirement for NO during ABA-induced stomatal closure in turgid and wilted leaves. Plant Cell Environ. 32, 46
57. Riemann, M., Dhakarey, R., Hazman, M., Miro, B., Kohli, A., Nick, P., 2015. Exploring jasmonates in the hormonal network of drought and salinity responses. Front. Plant Sci. 6, 1077. Rivero, R.M., Kojima, M., Gepstein, A., Sakakibara, H., Mittler, R., Gepstein, S., et al., 2007. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. U.S.A. 104, 19631
19636.

Plant Life under Changing Environment

References

457

Romero-Puertas, M.C., Sandalio, L.M., 2016. Nitric oxide level is self regulating and also regulates its ROS partners. Front. Plant Sci. 7, 316. Rosquete, M.R., Barbez, E., Kleine-Vehn, J., 2012. Cellular auxin homeostasis: gatekeeping is housekeeping. Mol. Plant 5, 772
786. Rushton, D.L., Tripathi, P., Rabara, R.C., Lin, J., Ringler, P., Boken, A.K., et al., 2012. WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol. J. 10, 2
11. Ryu, H., Cho, H., Kim, K., Hwang, I., 2010. Phosphorylation dependent nucleocytoplasmic shuttling of BES1 is a key regulatory event in brassinosteroid signaling. Mol. Cells 29, 283
290. Saeed, W., Naseem, S., Ali, Z., 2017. Strigolactones biosynthesis and their role in abiotic stress resilience in plants: a critical review. Front. Plant Sci. 8, 1487. Sah, S.K., Reddy, K.R., Li, J., 2016. Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 7, 571. Saini, S., Sharma, I., Pati, P.K., 2017. Integrating the knowledge of auxin homeostasis with stress tolerance in plants. In: Pandey, G.K. (Ed.), Mechanism of Plant Hormone Signaling Under Stress. John Wiley & Sons, Inc, Hoboken, NJ. Sakai, H., Honma, T., Aoyama, T., Sato, S., Kato, T., Tabata, S., et al., 2001. ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294, 1519
1521. Sakakibara, H., 2006. Cytokinins: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 57, 431
449. Sakakibara, H., 2010. Cytokinin biosynthesis and metabolism. In: Davies, P. (Ed.), Plant Hormones. Springer, The Netherlands. Sakuma, Y., Liu, Q., Dubouzet, J.G., Abe, H., Shinozaki, K., Yamaguchi-Shinozaki, K., 2002. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and coldinducible gene expression. Biochem. Biophys. Res. Commun. 290, 998
1009. Sakuma, Y., Maruyama, K., Qin, F., Osakabe, Y., Shinozaki, K., Yamaguchi-Shinozaki, K., 2006. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl. Acad. Sci. U.S.A. 103, 18822
18827. ˇ Salopek-Sondi, B., Pavlovi´c, I., Smolko, A., Samec, D., 2017. Auxin as a mediator of abiotic stress responses. In: Mechanism of Plant Hormone Signaling Under Stress, Wiley, pp. 1
36. Sanan-Mishra, N., Varanasi, S.P., Mukherjee, S.K., 2013. Micro-regulators of auxin action. Plant Cell Rep. 32, 733
740. Santiago, J., Dupeux, F., Betz, K., Antoni, R., Gonzalez-Guzman, M., Rodriguez, L., et al., 2012. Structural insights into PYR/PYL/RCAR ABA receptors and PP2Cs. Plant Sci. 182, 3
11. Santner, A., Estelle, M., 2009. Recent advances and emerging trends in plant hormone signalling. Nature 459, 1071. Santolini, J., Andre´, F., Jeandroz, S., Wendehenne, D., 2017. Nitric oxide synthase in plants: where do we stand? Nitric Oxide 63, 30
38. Sanz, L., Albertos, P., Mateos, I., Sa´nchez-Vicente, I., Lecho´n, T., Ferna´ndez-Marcos, M., et al., 2015. Nitric oxide (NO) and phytohormones crosstalk during early plant development. J. Exp. Bot. 66, 2857
2868. Schaller, G.E., Street, I.H., Kieber, J.J., 2014. Cytokinin and the cell cycle. Curr. Opin. Plant Biol. 21, 7
15. Schellingen, K., Van Der Straeten, D., Vandenbussche, F., Prinsen, E., Remans, T., Vangronsveld, J., et al., 2014. Cadmium-induced ethylene production and responses in Arabidopsis thaliana rely on ACS2 and ACS6 gene expression. BMC Plant Biol. 14, 214. Scherer, G.F., Ryu, S.B., Wang, X., Matos, A.R., Heitz, T., 2010. Patatin-related phospholipase A: nomenclature, subfamilies and functions in plants. Trends Plant Sci. 15, 693
700. Schommer, C., Palatnik, J.F., Aggarwal, P., Che´telat, A., Cubas, P., Farmer, E.E., et al., 2008. Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol. 6, e230. Schweighofer, A., Hirt, H., Meskiene, I., 2004. Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci. 9, 236
243. Seltmann, M.A., Stingl, N.E., Lautenschlaeger, J.K., Krischke, M., Mueller, M.J., Berger, S., 2010. Differential impact of lipoxygenase 2 and jasmonates on natural and stress-induced senescence in Arabidopsis. Plant Physiol. 152, 1940
1950. Seo, M., Koshiba, T., 2002. Complex regulation of ABA biosynthesis in plants. Trends Plant Sci. 7, 41
48. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H., Ohashi, Y., 1995. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270, 1988
1992.

Plant Life under Changing Environment

458

16. Phytohormonal signaling under abiotic stress

Seo, S., Sano, H., Ohashi, Y., 1999. Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell 11, 289
298. Seo, J.S., Joo, J., Kim, M.J., Kim, Y.K., Nahm, B.H., Song, S.I., et al., 2011. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J. 65, 907
921. Seto, Y., Sado, A., Asami, K., Hanada, A., Umehara, M., Akiyama, K., et al., 2014. Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc. Natl. Acad. Sci. U.S.A. 111, 1640
1645. Shan, C., Mei, Z., Duan, J., Chen, H., Feng, H., Cai, W., 2014. OsGA2ox5, a gibberellin metabolism enzyme, is involved in plant growth, the root gravity response and salt stress. PLos One 9, e87110. Sharan, A., Dkhar, J., Singla-Pareek, S.L., Pareek, A., 2017. Crosstalk between gibberellins and abiotic stress tolerance machinery in plants. In: Pandey, G.K. (Ed.), Mechanism of Plant Hormone Signaling Under Stress. John Wiley & Sons, Inc, Hoboken, NJ. Sharma, I., Kaur, N., Saini, S., Pati, P.K., 2013a. Emerging dynamics of brassinosteroids research. Biotechnology: Prospects and Applications. Springer, pp. 3
17. Sharma, R., Priya, P., Jain, M., 2013b. Modified expression of an auxin-responsive rice CC-type glutaredoxin gene affects multiple abiotic stress responses. Planta 238, 871
884. Sharma, E., Sharma, R., Borah, P., Jain, M., Khurana, J.P., 2015a. Emerging roles of auxin in abiotic stress responses. Elucidation of Abiotic Stress Signaling in Plants. Springer, pp. 299
328. Sharma, I., Bhardwaj, R., Pati, P.K., 2015b. Exogenous application of 28-homobrassinolide modulates the dynamics of salt and pesticides induced stress responses in an elite rice variety Pusa Basmati-1. J. Plant Growth Regul. 34, 509
518. Sharma, I., Kaur, N., Pati, P.K., 2017. Brassinosteroids: a promising option in deciphering remedial strategies for abiotic stress tolerance in rice. Front. Plant Sci. 8, 2151. Sharp, R., 2002. Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ. 25, 211
222. Shi, Y., Tian, S., Hou, L., Huang, X., Zhang, X., Guo, H., et al., 2012. Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24, 2578
2595. Shi, Y.-F., Wang, D.-L., Wang, C., Culler, A.H., Kreiser, M.A., Suresh, J., et al., 2015. Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol. Plant 8, 1350
1365. Siddiqui, M.H., Al-Whaibi, M.H., Basalah, M.O., 2011. Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248, 447
455. Simontacchi, M., Galatro, A., Ramos-Artuso, F., Santa-Marı´a, G.E., 2015. Plant survival in a changing environment: the role of nitric oxide in plant responses to abiotic stress. Front. Plant Sci. 6, 977. Singh, D., Laxmi, A., 2015. Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Front. Plant Sci. 6, 895. Singh, A.P., Dixit, G., Kumar, A., Mishra, S., Singh, P.K., Dwivedi, S., et al., 2016. Nitric Oxide Alleviated Arsenic Toxicity by Modulation of Antioxidants and Thiol Metabolism in Rice (Oryza sativa L.). Front. Plant Sci. 6, 1272. Singh, H.P., Kaur, S., Batish, D.R., Sharma, V.P., Sharma, N., Kohli, R.K., 2009. Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric oxide 20, 289
297. Skirycz, A., De Bodt, S., Obata, T., De Clercq, I., Claeys, H., De Rycke, R., et al., 2010. Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress. Plant Physiol. 152, 226
244. Smith, B.C., Marletta, M.A., 2012. Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling. Curr. Opin. Chem. Biol. 16, 498
506. Smith, S.M., Li, J., 2014. Signalling and responses to strigolactones and karrikins. Curr. Opin. Plant Biol. 21, 23
29. Sokolovski, S., Blatt, M.R., 2004. Nitric oxide block of outward-rectifying K1 channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol. 136, 4275
4284. Solano, R., Stepanova, A., Chao, Q., Ecker, J.R., 1998. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12, 3703
3714. Song, X., She, X., Wang, J., 2012. Inhibition of darkness-induced stomatal closure by ethylene involves a removal of hydrogen peroxide from guard cells of Vicia faba. Russ. J. Plant Physiol. 59, 372
380.

Plant Life under Changing Environment

References

459

Soundappan, I., Bennett, T., Morffy, N., Liang, Y., Stanga, J.P., Abbas, A., et al., 2015. SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 27, 3143
3159. Souri, Z., Karimi, N., Sandalio, L.M., 2017. Arsenic hyperaccumulation strategies: an overview. Front. Cell Dev. Biol. 5, 67. Stanga, J.P., Smith, S.M., Briggs, W.R., Nelson, D.C., 2013. SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol. 163, 318
330. Steber, C.M., McCourt, P., 2001. A role for brassinosteroids in germination in Arabidopsis. Plant Physiol. 125, 763
769. Strader, L.C., Chen, G.L., Bartel, B., 2010. Ethylene directs auxin to control root cell expansion. Plant J. 64, 874
884. Sun, S., Wang, H., Yu, H., Zhong, C., Zhang, X., Peng, J., et al., 2013. GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation. J. Exp. Bot. 64, 1637
1647. Sun, H., Bi, Y., Tao, J., Huang, S., Hou, M., Xue, R., et al., 2016a. Strigolactones are required for nitric oxide to induce root elongation in response to nitrogen and phosphate deficiencies in rice. Plant Cell Environ. 39, 1473
1484. Sun, H., Tao, J., Gu, P., Xu, G., Zhang, Y., 2016b. The role of strigolactones in root development. Plant Signal. Behav. 11, e1110662. Tada, Y., Spoel, S.H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., et al., 2008. Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952
956. Taj, G., Agarwal, P., Grant, M., Kumar, A., 2010. MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal. Behav. 5, 1370
1378. Takahashi, S., Yamasaki, H., 2002. Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett. 512, 145
148. Takahashi, Y., Ebisu, Y., Kinoshita, T., Doi, M., Okuma, E., Murata, Y., et al., 2013. bHLH transcription factors that facilitate K1 uptake during stomatal opening are repressed by abscisic acid through phosphorylation. Sci. Signal. 6, ra48. Available from: https://doi.org/10.1126/scisignal.2003760. Tanaka, Y., Sano, T., Tamaoki, M., Nakajima, N., Kondo, N., Hasezawa, S., 2005. Ethylene inhibits abscisic acidinduced stomatal closure in Arabidopsis. Plant Physiol. 138, 2337
2343. Tanaka, Y., Sano, T., Tamaoki, M., Nakajima, N., Kondo, N., Hasezawa, S., 2006. Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis. J. Exp. Bot. 57, 2259
2266. Tang, W., Kim, T.-W., Oses-Prieto, J.A., Sun, Y., Deng, Z., Zhu, S., et al., 2008. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557
560. Tang, N., Zhang, H., Li, X., Xiao, J., Xiong, L., 2012. Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol. 158, 1755
1768. Tang, J., Han, Z., Chai, J., 2016. Q&A: what are brassinosteroids and how do they act in plants? BMC Biol. 14, 113. Terrile, M.C., Parı´s, R., Caldero´n-Villalobos, L.I., Iglesias, M.J., Lamattina, L., Estelle, M., et al., 2012. Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J. 70, 492
500. Thaler, J.S., Stout, M.J., Karban, R., Duffey, S.S., 2001. Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol. Entomol. 26, 312
324. Theodoulou, F.L., Job, K., Slocombe, S.P., Footitt, S., Holdsworth, M., Baker, A., et al., 2005. Jasmonic acid levels are reduced in COMATOSE ATP-binding cassette transporter mutants. Implications for transport of jasmonate precursors into peroxisomes. Plant Physiol. 137, 835
840. Thu, N.B.A., Hoang, X.L.T., Truc, M.T.T., Sulieman, S., Thao, N.P., Thran, L.-S.P., 2017. Cytokinin signaling in plant response to abiotic stresses. In: Pandey, G.K. (Ed.), Mechanism of Plant Hormone Signaling Under Stress. John Wiley & Sons, Inc. Tognetti, V.B., Mu¨hlenbock, P., Van Breusegem, F., 2012. Stress homeostasis—the redox and auxin perspective. Plant Cell Environ. 35, 321
333. Tran, L.-S.P., Urao, T., Qin, F., Maruyama, K., Kakimoto, T., Shinozaki, K., et al., 2007. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 20623
20628.

Plant Life under Changing Environment

460

16. Phytohormonal signaling under abiotic stress

Tran, L.-S.P., Shinozaki, K., Yamaguchi-Shinozaki, K., 2010. Role of cytokinin responsive two-component system in ABA and osmotic stress signalings. Plant Signal. Behav. 5, 148
150. Trinh, N.N., Huang, T.L., Chi, W.C., Fu, S.F., Chen, C.C., Huang, H.J., 2014. Chromium stress response effect on signal transduction and expression of signaling genes in rice. Physiol. Plant. 150, 205
224. Tripathy, B.C., Oelmu¨ller, R., 2012. Reactive oxygen species generation and signaling in plants. Plant Signal. Behav. 7, 1621
1633. Turner, J.G., Ellis, C., Devoto, A., 2002. The jasmonate signal pathway. Plant Cell 14, S153
S164. Tuteja, N., 2007. Abscisic acid and abiotic stress signaling. Plant Signal. Behav. 2, 135
138. Tuteja, N., Sopory, S.K., 2008. Chemical signaling under abiotic stress environment in plants. Plant Signal. Behav. 3, 525
536. Tuteja, N., Gill, S.S., Trivedi, P.K., Asif, M.H., Nath, P., 2010. Plant growth regulators and their role in stress tolerance. Plant nutrition and abiotic stress tolerance I. Plant Stress 4, 1
18. Ubeda-Toma´s, S., Swarup, R., Coates, J., Swarup, K., Laplaze, L., Beemster, G.T., et al., 2008. Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat. Cell Biol. 10, 625. Ueguchi-Tanaka, M., Matsuoka, M., 2010. The perception of gibberellins: clues from receptor structure. Curr. Opin. Plant Biol. 13, 503
508. Umezawa, T., Nakashima, K., Miyakawa, T., Kuromori, T., Tanokura, M., Shinozaki, K., et al., 2010. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol. 51, 1821
1839. Upreti, K., Sharma, M., 2016. Role of plant growth regulators in abiotic stress tolerance. Abiotic Stress Physiology of Horticultural Crops. Springer, pp. 19
46. Urao, T., Miyata, S., Yamaguchi-Shinozaki, K., Shinozaki, K., 2000. Possible His to Asp phosphorelay signaling in an Arabidopsis two-component system. FEBS Lett. 478, 227
232. Uozu, S., Tanaka-Ueguchi, M., Kitano, H., Hattori, K., Matsuoka, M., 2000. Characterization of XET-related genes of rice. Plant Physiol. 122, 853
859. Vardhini, B.V., 2015. Brassinosteroids are potential ameliorators of heavy metal stresses in plants. Plant Metal Interaction. Elsevier, pp. 209
237. Vardhini, B.V., Anjum, N.A., 2015. Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system. Front. Environ. Sci. 2, 67. Verma, S., Nizam, S., Verma, P.K., 2013. Biotic and abiotic stress signaling in plants. Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 1. Springer, pp. 25
49. Verma, V., Ravindran, P., Kumar, P.P., 2016. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 16, 86. Veselov, D.S., Kudoyarova, G.R., Kudryakova, N.V., Kusnetsov, V.V., 2017. Role of cytokinins in stress resistance of plants. Russ. J. Plant Physiol. 64, 15
27. Vishwakarma, K., Upadhyay, N., Kumar, N., Yadav, G., Singh, J., Mishra, R.K., et al., 2017. Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant Sci. 8, 161. Vlot, A.C., Dempsey, D.M.A., Klessig, D.F., 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47, 177
206. Vriet, C., Russinova, E., Reuzeau, C., 2012. Boosting crop yields with plant steroids. Plant Cell 24, 842
857. Vysotskaya, L.B., Korobova, A.V., Veselov, S.Y., Dodd, I.C., Kudoyarova, G.R., 2009. ABA mediation of shoot cytokinin oxidase activity: assessing its impacts on cytokinin status and biomass allocation of nutrientdeprived durum wheat. Funct. Plant Biol. 36, 66
72. Walia, H., Wilson, C., Condamine, P., Liu, X., Ismail, A.M., Close, T.J., 2007. Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ. 30, 410
421. Wang, X., Chory, J., 2006. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313, 1118
1122. Wang, Y.H., Irving, H.R., 2011. Developing a model of plant hormone interactions. Plant Signal. Behav. 6, 494
500. Wang, R., Estelle, M., 2014. Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway. Curr. Opin. Plant Biol. 21, 51
58.

Plant Life under Changing Environment

References

461

Wang, Y., Mopper, S., Hasenstein, K.H., 2001a. Effects of salinity on endogenous ABA, IAA, JA, and SA in Iris hexagona. J. Chem. Ecol. 27, 327
342. Wang, Z.-Y., Seto, H., Fujioka, S., Yoshida, S., Chory, J., 2001b. BRI1 is a critical component of a plasmamembrane receptor for plant steroids. Nature 410, 380. Wang, K.L.-C., Li, H., Ecker, J.R., 2002. Ethylene biosynthesis and signaling networks. Plant Cell 14, S131
S151. Wang, D., Amornsiripanitch, N., Dong, X., 2006. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathogens 2, e123. Wang, L., Wang, Z., Xu, Y., Joo, S.H., Kim, S.K., Xue, Z., et al., 2009. OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J. 57, 498
510. Wang, R.-S., Pandey, S., Li, S., Gookin, T.E., Zhao, Z., Albert, R., et al., 2011. Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells. BMC Genomics 12, 216. Wang, F., Cui, X., Sun, Y., Dong, C.-H., 2013a. Ethylene signaling and regulation in plant growth and stress responses. Plant Cell Rep. 32, 1099
1109. Wang, Y., Sun, S., Zhu, W., Jia, K., Yang, H., Wang, X., 2013b. Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev. Cell 27, 681
688. Wang, Y., Wang, Y., Kai, W., Zhao, B., Chen, P., Sun, L., et al., 2014. Transcriptional regulation of abscisic acid signal core components during cucumber seed germination and under Cu21, Zn21, NaCl and simulated acid rain stresses. Plant Physiol. Biochem. 76, 67
76. Wang, L., Wang, B., Jiang, L., Liu, X., Li, X., Lu, Z., et al., 2015a. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27, 3128
3142. Wang, P., Zhu, J.-K., Lang, Z., 2015b. Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by S-nitrosylation of SnRK2 proteins. Plant Signal. Behav. 10, e1031939. Wang, X., Teng, Y., Zhang, N., Christie, P., Li, Z., Luo, Y., et al., 2017. Rhizobial symbiosis alleviates polychlorinated biphenyls-induced systematic oxidative stress via brassinosteroids signaling in alfalfa. Sci. Total Environ. 592, 68
77. Wang, Y.G., Fu, F.L., Yu, H.Q., Hu, T., Zhang, Y.Y., Tao, Y., et al., 2018. Interaction network of core ABA signaling components in maize. Plant Mol. Biol. 96, 245
263. Wani, S.H., Kumar, V., Shriram, V., Sah, S.K., 2016. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J. 4, 162
176. Wany, A., Gupta, K.J., 2018. Reactive oxygen species, nitric oxide production and antioxidant gene expression during development of aerenchyma formation in wheat. J. Plant Signal. Behav. 16, e1428515. Wasternack, C., Hause, B., 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111, 1021
1058. Waters, M.T., Scaffidi, A., Flematti, G.R., Smith, S.M., 2013. The origins and mechanisms of karrikin signalling. Curr. Opin. Plant Biol. 16, 667
673. Weiner, J.J., Peterson, F.C., Volkman, B.F., Cutler, S.R., 2010. Structural and functional insights into core ABA signaling. Curr. Opin. Plant Biol. 13, 495
502. Wendehenne, D., Pugin, A., Klessig, D.F., Durner, J., 2001. Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci. 6, 177
183. Werner, T., Schmu¨lling, T., 2009. Cytokinin action in plant development. Curr. Opin. Plant Biol. 12, 527
538. Werner, T., Nehnevajova, E., Ko¨llmer, I., Nova´k, O., Strnad, M., Kra¨mer, U., et al., 2010. Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22, 3905
3920. Weston, D.E., Elliott, R.C., Lester, D.R., Rameau, C., Reid, J.B., Murfet, I.C., et al., 2008. The pea DELLA proteins LA and CRY are important regulators of gibberellin synthesis and root growth. Plant Physiol. 147, 199
205. Wildermuth, M.C., Dewdney, J., Wu, G., Ausubel, F.M., 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562. Wilkinson, S., Davies, W.J., 2002. ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ. 25, 195
210. Willige, B.C., Isono, E., Richter, R., Zourelidou, M., Schwechheimer, C., 2011. Gibberellin regulates PIN-FORMED abundance and is required for auxin transport
dependent growth and development in Arabidopsis thaliana. Plant Cell 23, 2184
2195.

Plant Life under Changing Environment

462

16. Phytohormonal signaling under abiotic stress

Wilmowicz, E., Ke˛sy, J., Kopcewicz, J., 2008. Ethylene and ABA interactions in the regulation of flower induction in Pharbitis nil. J. Plant Physiol. 165, 1917
1928. Wohlbach, D.J., Quirino, B.F., Sussman, M.R., 2008. Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20, 1101
1117. Wolf, S., Mravec, J., Greiner, S., Mouille, G., Ho¨fte, H., 2012. Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Curr. Biol. 22, 1732
1737. Woodward, A.W., Bartel, B., 2005. Auxin: regulation, action, and interaction. Ann. Bot. 95, 707
735. Wu, Y., Zhang, D., Chu, J.Y., Boyle, P., Wang, Y., Brindle, I.D., et al., 2012. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 1, 639
647. Xia, X.-J., Wang, Y.-J., Zhou, Y.-H., Tao, Y., Mao, W.-H., Shi, K., et al., 2009. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol. 150, 801
814. Xia, K., Wang, R., Ou, X., Fang, Z., Tian, C., Duan, J., et al., 2012. OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 7, e30039. Xiang, Y., Tang, N., Du, H., Ye, H., Xiong, L., 2008. Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol. 148, 1938
1952. Xiong, L., Zhu, J.K., 2002. Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ. 25, 131
139. Xiong, L., Ishitani, M., Lee, H., Zhu, J.-K., 2001. The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13, 2063
2083. Xiong, H., Li, J., Liu, P., Duan, J., Zhao, Y., Guo, X., et al., 2014. Overexpression of OsMYB48-1, a novel MYBrelated transcription factor, enhances drought and salinity tolerance in rice. PLoS One 9, e92913. Xu, J., Wang, W., Yin, H., Liu, X., Sun, H., Mi, Q., 2010. Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326, 321. Xu, J., Wang, W., Sun, J., Zhang, Y., Ge, Q., Du, L., et al., 2011a. Involvement of auxin and nitric oxide in plant Cd-stress responses. Plant Soil 346, 107. Xu, Z.S., Chen, M., Li, L.C., Ma, Y.Z., 2011b. Functions and application of the AP2/ERF transcription factor family in crop improvement. J. Integr. Plant Biol. 53, 570
585. Yamada, Y., Umehara, M., 2015. Possible roles of strigolactones during leaf senescence. Plants 4, 664
677. Yamaguchi, S., 2008. Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 59, 225
251. Yan, S., Dong, X., 2014. Perception of the plant immune signal salicylic acid. Curr. Opin. Plant Biol. 20, 64
68. Yan, Y., Christensen, S., Isakeit, T., Engelberth, J., Meeley, R., Hayward, A., et al., 2012. Disruption of OPR7 and OPR8 reveals the versatile functions of jasmonic acid in maize development and defense. Plant Cell 24, 1420
1436. Yan, Z., Chen, J., Li, X., 2013. Methyl jasmonate as modulator of Cd toxicity in Capsicum frutescens var. fasciculatum seedlings. Ecotoxicol. Environ. Saf. 98, 203
209. Yang, S.F., Hoffman, N.E., 1984. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35, 155
189. Yang, T., Poovaiah, B., 2002. A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J. Biol. Chem. 277, 45049
45058. Yang, W., Devaiah, S.P., Pan, X., Isaac, G., Welti, R., Wang, X., 2007. AtPLAI is an acyl hydrolase involved in basal jasmonic acid production and Arabidopsis resistance to Botrytis cinerea. J. Biol. Chem. 282, 18116
18128. Yang, W., Liu, X.-D., Chi, X.-J., Wu, C.-A., Li, Y.-Z., Song, L.-L., et al., 2011. Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233, 219
229. Yang, Y., Ma, C., Xu, Y., Wei, Q., Imtiaz, M., Lan, H., et al., 2014. A zinc finger protein regulates flowering time and abiotic stress tolerance in chrysanthemum by modulating gibberellin biosynthesis. Plant Cell 26, 2038
2054. Yang, W., Zhang, W., Wang, X., 2017. Post-translational control of ABA signalling: the roles of protein phosphorylation and ubiquitination. Plant Biotechnol. J. 15, 4
14.

Plant Life under Changing Environment

References

463

Ye, H., Li, L., Yin, Y., 2011. Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways. J. Integr. Plant Biol. 53, 455
468. Yevdakova, N.A., Motyka, V., Malbeck, J., Tra´vnı´cˇ kova´, A., Nova´k, O., Strnad, M., et al., 2008. Evidence for importance of tRNA-dependent cytokinin biosynthetic pathway in the moss Physcomitrella patens. J. Plant Growth Regul. 27, 271. Yin, Y., Wang, Z.-Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., et al., 2002. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109, 181
191. Yoneyama, K., Xie, X., Kim, H.I., Kisugi, T., Nomura, T., Sekimoto, H., et al., 2012. How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235, 1197
1207. Yoon, J.Y., Hamayun, M., Lee, S.-K., Lee, I.-J., 2009. Methyl jasmonate alleviated salinity stress in soybean. J. Crop Sci. Biotechnol. 12, 63
68. Yoshida, R., Umezawa, T., Mizoguchi, T., Takahashi, S., Takahashi, F., Shinozaki, K., 2006. The regulatory domain of SRK2E/OST1/SnRK2. 6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J. Biol. Chem. 281, 5310
5318. Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., et al., 2010. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61, 672
685. Yoshida, T., Mogami, J., Yamaguchi-Shinozaki, K., 2014. ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr. Opin. Plant Biol. 21, 133
139. Yoshida, T., Fujita, Y., Maruyama, K., Mogami, J., Todaka, D., Shinozaki, K., et al., 2015. Four Arabidopsis AREB/ ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ. 38, 35
49. ˇ ´ , M., Mrı´zova´, K., Fre´bort, I., Galuszka, P., 2013. Genetic engineering of Zalaba´k, D., Pospı´sˇ ilova´, H., Smehilova cytokinin metabolism: prospective way to improve agricultural traits of crop plants. Biotechnol. Adv. 31, 97
117. Zawaski, C., Busov, V.B., 2014. Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in Populus trees. PLoS One 9, e86217. Zazimalova, E., Murphy, A.S., Yang, H., Hoyerova´, K., Hoˇsek, P., 2010. Auxin transporters—why so many? Cold Spring Harbor Perspect. Biol. 2, a001552. Zhang, J.Y., Broeckling, C.D., Blancaflor, E.B., Sledge, M.K., Sumner, L.W., Wang, Z.Y., 2005. Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J. 42, 689
707. Zhang, J., Jia, W., Yang, J., Ismail, A.M., 2006. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res. 97, 111
119. Zhang, A., Zhang, J., Zhang, J., Ye, N., Zhang, H., Tan, M., et al., 2010. Nitric oxide mediates brassinosteroidinduced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol. 52, 181
192. Zhang, S.-W., Li, C.-H., Cao, J., Zhang, Y.-C., Zhang, S.-Q., Xia, Y.-F., et al., 2009a. Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3. 13 activation. Plant Physiol. 151, 1889
1901. Zhang, S., Cai, Z., Wang, X., 2009b. The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 4543
4548. Zhang, L., Li, Z., Quan, R., Li, G., Wang, R., Huang, R., 2011. An AP2 domain-containing gene, ESE1, targeted by the ethylene signaling component EIN3 is important for the salt response in Arabidopsis. Plant Physiol. 157, 854
865. Zhang, C., Bai, M.-y, Chong, K., 2014a. Brassinosteroid-mediated regulation of agronomic traits in rice. Plant Cell Rep. 33, 683
696. Zhang, J., Yu, J., Wen, C.-K., 2014b. An alternate route of ethylene receptor signaling. Front. Plant Sci. 5, 648. Zhang, Y., Ruyter-Spira, C., Bouwmeester, H.J., 2015. Engineering the plant rhizosphere. Curr. Opin. Biotechnol. 32, 136
142. Zhang, F.-P., Sussmilch, F., Nichols, D.S., Cardoso, A.A., Brodribb, T.J., McAdam, S.A., 2018. Leaves, not roots or floral tissue, are the main site of rapid, external pressure-induced ABA biosynthesis in angiosperms. J. Exp. Bot. 69 (5), 1261
1267.

Plant Life under Changing Environment

464

16. Phytohormonal signaling under abiotic stress

Zhang, N., Yin, Y., Liu, X., Tong, S., Xing, J., Zhang, Y., et al., 2017. The E3 ligase TaSAP5 alters drought stress responses by promoting the degradation of DRIP proteins. Plant Physiol. 175, 1878
1892. 01319.2017. Zhao, Y., 2010. Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biol. 61, 49
64. Zhao, B., Li, J., 2012. Regulation of brassinosteroid biosynthesis and inactivation. J. Integr. Plant Biol. 54, 746
759. Zhao, Y., Christensen, S.K., Fankhauser, C., Cashman, J.R., Cohen, J.D., Weigel, D., et al., 2001. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291, 306
309. Zhao, L.-H., Zhou, X.E., Wu, Z.-S., Yi, W., Xu, Y., Li, S., et al., 2013. Crystal structures of two phytohormone signal-transducing α/β hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res. 23, 436. Zhao, L.-H., Zhou, X.E., Yi, W., Wu, Z., Liu, Y., Kang, Y., et al., 2015. Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3. Cell Res. 25, 1219. Zhao, P., Lu, G.H., Yang, Y.H., 2017. Salicylic acid signaling and its role in responses to stresses in plants. In: Mechanism of Plant Hormone Signaling Under Stress, Wiley, pp. 413
441. Zheng, C., Jiang, D., Liu, F., Dai, T., Liu, W., Jing, Q., et al., 2009. Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ. Exp. Bot. 67, 222
227. Zheng, X.Y., Spivey, N.W., Zeng, W., Liu, P.P., Fu, Z.Q., Klessig, D.F., et al., 2012. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11, 587
596. Zhou, F., Lin, Q., Zhu, L., Ren, Y., Zhou, K., Shabek, N., et al., 2013a. D14
SCF D3-dependent degradation of D53 regulates strigolactone signalling. Nature 504, 406. Zhou, Z.S., Yang, S.N., Li, H., Zhu, C.C., Liu, Z.P., Yang, Z.M., 2013b. Molecular dissection of mercury-responsive transcriptome and sense/antisense genes in Medicago truncatula. J. Hazard. Mater. 252, 123
131. Zhou, M., Wang, W., Karapetyan, S., Mwimba, M., Marque´s, J., Buchler, N.E., et al., 2015. Redox rhythm reinforces the circadian clock to gate immune response. Nature 523, 472
476. Zhu, Z., An, F., Feng, Y., Li, P., Xue, L., Mu, A., et al., 2011. Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc. Natl. Acad. Sci. U.S. A. 108, 12539
12544. Zhu, J.Y., Sae-Seaw, J., Wang, Z.Y., 2013. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802
809. Zhu, X., Qi, L., Liu, X., Cai, S., Xu, H., Huang, R., et al., 2014. The wheat ethylene response factor transcription factor pathogen-induced ERF1 mediates host responses to both the necrotrophic pathogen Rhizoctonia cerealis and freezing stresses. Plant Physiol. 164, 1499
1514. Zong, X.-j, Li, D.-P., Gu, L.-k, Li, D.-Q., Liu, L.-x, Hu, X.-l, 2009. Abscisic acid and hydrogen peroxide induce a novel maize group C MAP kinase gene, ZmMPK7, which is responsible for the removal of reactive oxygen species. Planta 229, 485. Zottini, M., Formentin, E., Scattolin, M., Carimi, F., Lo Schiavo, F., Terzi, M., 2002. Nitric oxide affects plant mitochondrial functionality in vivo. FEBS Lett. 515, 75
78. Zubo, Y.O., Yamburenko, M.V., Selivankina, S.Y., Shakirova, F.M., Avalbaev, A.M., Kudryakova, N.V., et al., 2008. Cytokinin stimulates chloroplast transcription in detached barley leaves. Plant Physiol. 148, 1082
1093. Zwack, P.J., Rashotte, A.M., 2015. Interactions between cytokinin signalling and abiotic stress responses. J. Exp. Bot. 66, 4863
4871.

Further reading Abat, J.K., Deswal, R., 2009. Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9, 4368
4380. Bartels, D., Sunkar, R., 2005. Drought and salt tolerance in plants. Crit. Rev. Plant Sci. 24, 23
58. Boudsocq, M., Barbier-Brygoo, H., Laurie`re, C., 2004. Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J. Biol. Chem. 279, 41758
41766. Bu, Q., Lv, T., Shen, H., Luong, P., Wang, J., Wang, Z., et al., 2014. Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiol. 164, 424
439.

Plant Life under Changing Environment

Further reading

465

Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., Abrams, S.R., 2010. Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651
679. Feechan, A., Kwon, E., Yun, B.W., Wang, Y., Pallas, J.A., Loake, G.J., 2005. A central role for S-nitrosothiols in plant disease resistance. Proc. Natl. Acad. Sci. U.S.A. 102, 8054
8059. Fro¨hlich, A., Durner, J., 2011. The hunt for plant nitric oxide synthase (NOS): is one really needed? Plant Sci. 181, 401
404. Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Page`s, V., Dun, E.A., Pillot, J.-P., et al., 2008. Strigolactone inhibition of shoot branching. Nature 455, 189. Goodspeed, D., Chehab, E.W., Min-Venditti, A., Braam, J., Covington, M.F., 2012. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc. Natl. Acad. Sci. U.S.A. 109, 4674
4677. Ivanchenko, M.G., Muday, G.K., Dubrovsky, J.G., 2008. Ethylene
auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J. 55, 335
347. Khan, N.A., Syeed, S., Masood, A., Nazar, R., Iqbal, N., 2010. Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress. Int. J. Plant Biol. 1 (1), e1. Available from: https://doi.org/10.4081/pb.2010.e1. Khan, M.I.R., Syeed, S., Nazar, R., Anjum, N.A., 2012a. An insight into the role of salicylic acid and jasmonic acid in salt stress tolerance. Phytohormones and Abiotic Stress Tolerance in Plants. Springer, pp. 277
300. Kim, E.H., Kim, Y.S., Park, S.-H., Koo, Y.J., Do Choi, Y., Chung, Y.-Y., et al., 2009. Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol. 149, 1751
1760. ´ Kulik, A., Wawer, I., Krzywinska, E., Bucholc, M., Dobrowolska, G., 2011. SnRK2 protein kinases—key regulators of plant response to abiotic stresses. Omics 15, 859
872. Liu, Y., Yin, Z., Yu, J., Li, J., Wei, H., Han, X., et al., 2012. Improved salt tolerance and delayed leaf senescence in transgenic cotton expressing the Agrobacterium IPT gene. Biol. Plant. 56, 237
246. Liu, L., Sonbol, F.-M., Huot, B., Guo, Y., Withers, J., Mwimba, M., et al., 2014. Salicylic acid receptors activate jasmonic acid signaling through a non-canonical pathway to promote effector-triggered immunity. Nat. Commun. 7, 1
10. Miura, K., Tada, Y., 2014. Regulation of water, salinity, and cold stress responses by salicylic acid. Front. Plant Sci. 5, 4. Miyawaki, K., Matsumoto-Kitano, M., Kakimoto, T., 2004. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 37, 128
138. Nakashima, K., Yamaguchi-Shinozaki, K., 2013. ABA signaling in stress-response and seed development. Plant Cell Rep. 32, 959
970. Nazar, R., Iqbal, N., Syeed, S., Khan, N.A., 2011. Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J. Plant Physiol. 168, 807
815. Negi, S., Sukumar, P., Liu, X., Cohen, J.D., Muday, G.K., 2010. Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J. 61, 3
15. Palmieri, M.C., Lindermayr, C., Bauwe, H., Steinhauser, C., Durner, J., 2010. Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiol. 152, 1514
1528. Pandey, S., Nelson, D.C., Assmann, S.M., 2009. Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136, 136
148. Qiu, Z.B., Guo, J.L., Zhu, A.J., Zhang, L., Zhang, M.M., 2014. Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Exotoxicol. Environ. Saf. 104, 202
208. Raghavendra, A.S., Gonugunta, V.K., Christmann, A., Grill, E., 2010. ABA perception and signalling. Trends Plant Sci. 15, 395
401. Santiago, J., Rodrigues, A., Saez, A., Rubio, S., Antoni, R., Dupeux, F., et al., 2009. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 60, 575
588. Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., et al., 2001. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13, 61
72. Seo, H.S., Song, J.T., Cheong, J.-J., Lee, Y.-H., Lee, Y.-W., Hwang, I., et al., 2001. Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc. Natl. Acad. Sci. U.S.A. 98, 4788
4793.

Plant Life under Changing Environment

466

16. Phytohormonal signaling under abiotic stress

Seto, Y., Yamaguchi, S., 2014. Strigolactone biosynthesis and perception. Curr. Opin. Plant Biol. 21, 1
6. Stamm, P., Kumar, P.P., 2010. The phytohormone signal network regulating elongation growth during shade avoidance. J. Exp. Bot. 61, 2889
2903. ´ ´ ˙ Stroinski, A., Chadzinikolau, T., Gizewska, K., Zielezinska, M., 2010. ABA or cadmium induced phytochelatin synthesis in potato tubers. Biol. Plant. 54, 117
120. Su, Y.-H., Liu, Y.-B., Zhang, X.-S., 2011. Auxin
cytokinin interaction regulates meristem development. Mol. Plant 4, 616
625. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., et al., 2008. Inhibition of shoot branching by new terpenoid plant hormones. Nature 455, 195. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., Yamaguchi-Shinozaki, K., 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. U.S.A. 97, 11632
11637. Urao, T., Yamaguchi-Shinozaki, K., Urao, S., Shinozaki, K., 1993. An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5, 1529
1539. Wen, X., Zhang, C., Ji, Y., Zhao, Q., He, W., An, F., et al., 2012. Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Res. 22, 1613. Yamaguchi-Shinozaki, K., Shinozaki, K., 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781
803. Zhang, D.-P., 2016. Abscisic Acid: Metabolism, Transport and Signaling. Springer. Zhou, X., Liu, Q., Xie, F., Wen, C.-K., 2007. RTE1 is a Golgi-associated and ETR1-dependent negative regulator of ethylene responses. Plant Physiol. 145, 75
86. Zhu, J.-K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247
273.

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C H A P T E R

17 Role of sRNAs in abiotic stress tolerance Anuradha Patel1, Sanjesh Tiwari1, Madhulika Singh2 and Sheo Mohan Prasad1 1

Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India 2Centre of Advance Studies, Department of Botany, Banaras Hindu University, Varanasi, India

17.1 Introduction Any external factors either biotic or abiotic that significantly reduced the plants’ ability to convert light energy into biomass are studied under a broad category termed stresses that negatively influence the metabolic activities of plants (Grime, 1977). Along with biotic and abiotic stresses, overgrowing population also caused a lot of pressure on agricultural fields to fulfill the food demand, but the crops productivity was not increased in such manner as population increased. In natural environment, primary producers, that is, plants face a number of adverse environmental conditions such as high salinity, drought, cold, and heat that limits the biomass production and yield of staple food crops; hence, it is a global concern to fulfill the food demand (Thakur et al., 2010; Shanker and Venkateswarlu, 2011; Ahmad et al., 2012; Mantri et al., 2012). Various anthropogenic activities contribute to the abiotic stress that changes the climate of environment that causes threat to food security. These adverse environmental changes hamper the various physiological and metabolic factors, which result in death of plants. A physiological alteration under abiotic stresses includes growth inhibition associated with photosynthetic pigment loss, decreased whole-cell oxygen evolution (photosynthesis), and significant increase in oxygen consumption (Singh et al., 2016; Singh et al., 2018). Plants stimulate various adoptive changes in response to abiotic stresses at physiological, cellular and molecular level or through genetic regulation or reprogramming the expression of gene. Physiological adaptation includes change in protein modification at transcriptional level as well as at posttranslational level that leads the change in particular phenotype (Moldovan et al., 2010)

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© 2020 Elsevier Inc. All rights reserved.

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that significantly avoids the stressful conditions. One such approach is through the modification in gene expression and also through the activity of sRNAs, which switches on protective mechanisms, that is, the genes that involve in defense systems are upregulated and gens that involve in toxicity are downregulated (Ku et al., 2015). Role of proteomics as stress-tolerance mechanism are well known, whereas the role of sRNA as stress regulators is an emerging molecular tool (Carrington and Ambros, 2003). Further, due to the development of modern molecular techniques, molecular mechanisms in plants give much more attention to identify the stress-responsive proteins and their regulatory gene networks under posttranslational level. In this line, small noncoding RNAs (sRNAs) are considered posttranscriptional regulatory factor in gene regulation under adverse environmental factors and involved in plant development (Dalmay et al., 2000; Hutvagner et al., 2000). In molecular world, RNAs are basically categorized into two into transfer RNA and ribosomal RNA (Baulcombe, 2004; Sunkar et al., 2005), and the only difference in sRNAs from other forms of RNAs is relatively small size of genome (20
30 nt) as well as having capacity to make complex with argonaute (AGO) family proteins considered key components of RISC (RNA-induced silencing complex) (Mette et al., 2000; Matzke et al., 2009). Among various types of sRNA, two are major, that is, microRNAs (miRNAs) and small interfering RNAs (siRNAs) that actively mediate the gene regulation, splicing, DNA methylation, chromatin, protein, and nucleotide modification (Law and Jacobsen, 2010; Burkhart et al., 2011) and sRNA-mediated gene silencing termed RNA interference (RNAi) (Kamthan et al., 2015). RNAi significantly inhibits the process of transcription or translation by sequence-specific gene regulation initiated by dsRNA and frequently presents in plants as well as in animals, fungi, and ciliates (Baulcombe, 2000; Matzke et al., 2001). The present time is totally dependent on crop improvement techniques under adverse environmental conditions by use of various molecular approaches and among them RNAi is considered an important tool of genetic engineering and functional genomics. In this chapter, we briefly describe the biogenesis of sRNA and their pivotal role against abiotic stress tolerance.

17.2 sRNA Climate change due to abiotic factors significantly reduced the crop yields around the globe, but at the same time, plants evolve some adaptive mechanisms to overcome the stress conditions that involve the gene regulation at transcriptional and posttranslational levels (Shukla et al., 2008). Plants possess a distinct class of noncoding regulatory RNAs, which regulates various biological and physiological processes; however, plant system encompasses several metabolic pathways itself, which leads to the synthesis of sRNAs (Fig. 17.1). On the basis of biogenesis, sRNAs have been classified into miRNAs and siRNAs. Among them, the length of miRNAs is 21
24 nucleotide sequence and forms from RNAs by forming base-paired hairpin structures (Noman and Aqeel, 2017; Noman et al., 2017) and participates in the expression of target genes by binding to reverse complementary sequences, resulting in cleavage of the target RNAs (Khraiwesh et al., 2012). Contrary to this, siRNAs are derived either by dsRNAs or by DNA methylation at target sequences and require RNA-dependent RNA polymerase (RDRs) (Devert et al., 2015).

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17.4 Mechanism of sRNA-mediated gene regulation

Synthesis of sRNAs

dsRNA

Single nucleotide precursor of specific nucleotides (64–303) nt

siRNA duplex

Nucleus

Pri-miRNA

FIGURE 17.1 Schematic representation of sRNA synthesis in plants.

AGO RISC complex

Dorsha Pasha

Pre-miRNA miRNA

Export to cytosol

Pre-miRNA dicer

siRNA/miRNA complex

RISC

miRNA duplex

siRNAs

Removal of hairpin structure

Sliced mRNA

Further, siRNAs present in various forms in plants that are trans-acting siRNAs (ta-siRNAs), heterochromatic siRNAs, natural antisense transcript-derived siRNAs, and long siRNAs (Huang et al., 2016), which play pivotal role in growth and development against stress responses.

17.3 Biogenesis and mechanism of action of sRNAs sRNAs in plants are processed from single-stranded precursors having 64
303 nucleotides sequence-like hairpin structure, whereas in animals the length of precursors lies in the range of 60
70 nucleotides (Lim, 2003). The precursors of sRNAs are regulated by RNA polymerase II (RNA pol II). sRNA precursors are of both the origin exogenously synthesized from external cells and triggered gene and endogenously with in host cell (Bartel and Bartel, 2003; Carthew and Sontheimer, 2009). The precursors of sRNAs’ synthesis are usually double stranded and distinctive and play an important role in generation of different types of siRNAs as Ra-siRNAs and ta-siRNAs differed only on the basis of precursors (Kim, 2005); however, one is generated from repetitive sequences and other is from nucleolar RNA precursors. Processing and genesis of sRNAs involves the function of DNA-dependent RNA polymerase (RNA pol IV), which transcribes ssRNA precursors (Herr, 2005).

17.4 Mechanism of sRNA-mediated gene regulation Gene regulation via sRNA mainly involves four basic mechanisms: (1) cleavage of mRNA by endonuclease, (2) repression of protein synthesis, (3) transcriptional repression via DNA modification, and (4) histone modification that eliminates DNA. sRNA mediates

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gene silencing is known as posttranscriptional gene silencing (PTGS) in plants because it occurs at transcriptional level (Meister and Tuschl, 2004).

17.4.1 Transcriptional gene silencing It is a process by which transcription is repressed and stably affects the transposons, structure of chromosomes and also suppresses certain protein-coding genes (Nishimura et al., 2012). Cell-division events, such as mitosis and meiosis, actively participate in transcriptional gene silencing (TGS) in plants and are achieved through DNA modification (Law and Jacobsen, 2010). During the process of transcription, inhibition occurs at level of DNA methylation induced by sRNA (Baulcombe, 2004), and the phenomenon is called TGS. Moreover, this is also considered homology-dependent gene silencing due to similar nucleotide sequences between promoter and sRNA (Mette et al., 2000). RNA-directed DNA methylation first reported in transgenic tobacco during replication in which cDNA of viroid genome in the host nuclear genome (Wassenegger et al., 1994). Further, methylation of promoter region of cDNA cleaved by the enzyme leads to the formation of sRNAs. DNA methylation resulted in the modification of nucleotide sequences by enzymatic cytosine methylation, which is a universal phenomenon that occurs in plants as well as in animals (Vanyushin, 2006). DNA modification plays an important role in stress tolerance, inactivation of transposons and regulates the growth and development. DNA methylation is an enzymatic process that involves DNA methyltransferases, histone methyltransferases, chromatin remodeling factors, and proteins regulating different methylation stages, which are either RNA directed or RNA independent (Marenkova and Deineko, 2010). Methylation of histone protein lies in position 9 of lysine residue (H3K9me2) that significantly changes the confirmation of chromatin into repressive confirmation, which mediates the hypermethylation of cytosines (Law and Jacobsen, 2010). Furthermore, in Arabidopsis, histone modification via DNA methylation is absent, so in such cases the TGS is mediated by Morpheus molecule 1 (Vaillant et al., 2006). A number of studies have performed to show the relationship between TGS and abiotic stresses, and in Arabidopsis, ability of salt tolerance found to be decreased concurred with inhibition in DNA methylation at cytosine by 5-azacytidine treatment (Boyko et al., 2010). In Pinus persica, DNA methylation mediated by a number of cold-responsive miRNA targets the stress-responsive genes (Barakat et al., 2012).

17.4.2 Posttranscriptional gene silencing sRNA categorized into two major groups mainly miRNA and endogenous siRNA differs in their mode of action and biogenesis form different precursors. Precursors of miRNA are self-complementary, forming a hairpin-like loop, while siRNA precursors are complementary and double stranded. Further biogenesis of these sRNA is quite similar with each other (Barakat et al., 2012; Meister, 2013) and enzymatically controlled, that is, RNA polymerase II, IV, and V (Zheng et al., 2009). The precursors of sRNA finally cut into single-stranded miRNA and siRNA by dicer-like (DCL) proteins (Gasciolli et al., 2005). Later, cleaved single-stranded miRNAs and siRNAs are associated with argonaute (AGO) proteins and form RISC, and inhibition in transcription or translation occurs due to inhibition

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in RISC (Takeda et al., 2008). In eukaryotes, sRNA pathway is influenced by several factors or proteins such as RNase III, argonaute (AGO). Among these, RNase III plays a very important role consist of Dicer and Dorsha. Both proteins have a catalytic site and a dsRNAbinding site and helicase property retained in Dicer in form of DExH RNA helicase/ATPase domain. Dicer cleaves the dsRNA into RNA duplexes. Furthermore, Dorsha forms a short hairpin-like structure (pre-miRNA) due to cleavage of primary transcript miRNA. Argonaute (Ago) proteins are basic in nature having a molecular weight of 100 kDa and contain two domains mainly PAZ and PIWI domains. PAZ is 130 AA long and interacts with 30 of dsRNA due to its present in the center of proteins (Song et al., 2003; Lingel et al., 2004), while PIWI is 300 AA long and shows similarity with RNase H (Song et al., 2004). Ago proteins directly interact with sRNA and forms RISC, miRNP, or RNA-induced initiation of transcriptional silencing complex (RITS).

17.5 Role of mRNAs in stress tolerance For enduring under abiotic stress conditions, plants through modified gene expression at transcriptional or translational trigger a rearrangement of gene to turn on defensive mechanisms. Transcriptional reprogramming is an important pathway to activate the adaptation processes under stress conditions, and sRNAs play an important role in the regulation of gene expressions (Gehan et al., 2015). sRNAs are short nucleotide sequence about (22
25 nucleotides) which does not undergo the process of translation, that is, protein formation, but regulates various biological and developmental processes (Ku et al., 2015). In plants such as Nicotiana tabacum, Solanum lycopersicum, and Arabidopsis, short and unique length sRNAs were discovered, which show active involvement in PTGS (Dalmay et al., 2000). These short sequences were later termed siRNAs. Plant siRNAs are more different than miRNAs on the basis of their size, structures of precursors, origin, and functions. Jones-Rhoades and Bartel (2004) reported for the first time the role of miRNAs (miR395) in Arabidopsis thaliana, which was found to target gene encoding for ATP sulfurylases and antioxidant (SOD), and they reported that various environmental factors can induce changes in the expression of (miR395) (Fig. 17.2). miRNAs mainly target the ATP sulfurylases, which are involved in sulfur metabolism (Jones-Rhoades and Bartel, 2004). miR395 regulates the process of sulfur metabolism and also targets the AST68 that encodes for sulfate transporter (Allen et al., 2004). Sunkar and Zhu (2004) cloned short RNAs from Arabidopsis seedlings under stress condition and identified several miRNAs with differential gene expression such as abiotic stresses including temperature, salinity, and treatments of phytohormones as miR393 was sturdily upregulated, miR397b and miR402 were slightly upregulated by stress, while miR319c was only induced by under cold conditions; however, under stress condition, miR389a was downregulated (Fig. 17.2; Table 17.1).

17.6 Role of small interfering RNAs in defense against pathogen Pathogen (bacteria, fungi, viruses, and microbes) infection causes substantial losses to crop production, which in turn disturbs the food and supply demand (Zaynab et al., 2017).

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Application of sRNAs in plants Promotes hormonal signaling

Promotes secondary metabolites synthesis Stimulates developmental process in plants, that is, flowering

Improves nutritional quality of plants

Improves nutritional quality of plants

Tolerance against various abiotic and biotic stresses

Microorganism and viruses

FIGURE 17.2

Insecticide Fungicide

Improves plant height, promotes branching, and changes leaf morphology

Modification in histone structure

Improves rate of photosynthesis

Schematic representation of application of sRNA in plants.

To overcome these indemnities, plants through different pathways of transcriptional process implicate the synthesis of sRNAs (both siRNAs and miRNAs), and these serve major role in defense against pathogen attack. sRNAs provide immunity (Weiberg and Jin, 2015; Wang and Chekanova, 2016). sRNA pathways involve the synthesis of multiple proteins that initiate the protecting response, which are (1) endoribonuclease—a dicer (DCL) involved in promoting sRNAs’ synthesis, (2) argonautes (AGOs)—involved in suppression of gene and regulate the immune responses, and (3) RDRs—important role in generation of (dsRNA) precursor (Islam et al., 2017). A. thaliana genome encodes four proteins that have been reported to be involved in miRNA synthesis pathway, and out of these four, DCL1 is important one as it has direct involvement in miRNA genesis, and DCL4 is mainly involved in providing resistance against pathogen attack (Nicaise, 2014). Zvereva and Pooggin (2012) reported that six RDRs are found in A. thaliana in which RDR6 regulates the synthesis of (siRNAs and ta-siRNAs) and antiviral proteins (SGS3), thus inferring the important role of siRNAs in protecting against pathogen attack.

17.7 Role of sRNAs (lncRNAs—a type) in vernalization Vernalization is a process of plants in which induction of flower is induced by prolonged cold of winter, or by an artificial equivalent (Song et al., 2013). It is regulatory Plant Life under Changing Environment

TABLE 17.1 abiotic stress.

Different forms of sRNA and their role in plants associated with target gene under biotic and

S. no Plant name

sRNAs

Role in plant

Targeted gene

References

1.

Brassica napus

miR1885 Protection against virus infection (TuMV)

TIR
NBS
LRR

Wroblewski et al. (2007)

2.

Solanum lycopersicum

miR482

Protection against virus and viroid infection (TCV, CMN, and TRF)

NBS
LRR

Shivaprasad et al. (2012)

3.

Oryza sativa

miR168

AGO1

4.

Arabidopsis thaliana

Defense against pathogen attack RSV, RDV

Ouyang et al. (2014) Bortolamiol et al. (2007)

5.

Nicotiana benthamiana

6.

A. thaliana

miR167 miR393

Protection against bacterial infection caused by Pseudomonas syringae

7.

Citrus

miR393

Protection against bacterial infection caused by Candidatus liberibacter

ARF 8 ARF 6 T1R1 AFB3 PHOT 2

Fahlgren et al. (2007) Zhang et al. (2011) Zhao et al. (2013)

8.

A. thaliana

lncRNAs Regulates flowering time and modification of histone protein

COLDAIR (cold-assisted Heo and Sung intronic noncoding RNAs) (2011a,b)

9.

A. thaliana

lncRNAs Regulates flowering time and promoter interference

COOLAIR (cold-induced long antisense intragenic RNAs)

Swiezewski et al. (2009)

10. O. sativa

lncRNAs Promotes fertility

LDMAR-(P/TMS12-1) long day-specific malefertility-associated RNA

Zhao et al. (2013) Ding et al. (2012)

11. Hordeum vulgare

lncRNAs Promotes the synthesis of cell wall, SiRNAs precursor

HvCesA6 lnc-NAT

Held et al. (2008)

12. Petunia hybrida

SiRNAs

SHO lnc-NAT Petunia

Zubko and Meyer (2007)

13. Glycine max

lncRNAs Promotes nodule formation and localization of protein

GmENOD40

Yang et al. (1993)

14. Medicago truncatula

lncRNAs Promotes nodule formation and localization of protein

MtENOD40

Sousa et al. (2001)

15. A. thaliana

tasiR289

Insufficient O2 availability condition, At1g15940 or hypoxia At1g51670

16. Triticum aestivum

SiRNAs

Resistance under heat stress and dehydrated condition

Promotes cytokinin synthesis and degradation of dsRNA




Moldovan (2010) Yao (2010)

Promotes growth under cold, heat, and NaCl stress 17. Craterostigma plantagineum

SiRNAs

Resistance under stressful environment

Y11822

Hilbricht (2008)

TCV, turnip crinkle virus; CMN, canine minute virus; TRF, tRNA fragments; TIR- toll/mammalian interleukin-1 receptor; NBS, nucleotide binding site; LRR, lucine rich repeat; RSV, respiratory syncytial virus; RDV, rice dwarf virus

474

17. Role of sRNAs in abiotic stress tolerance

processes that involve sRNAs in regulation of gene responsible for the development of flowering locus (FLC) (He, 2012). FLC gene is a complex locus, which consists of two types of lncRNAs, one is transcribed in antisense orientation called COOLAIR (cold-induced long antisense intragenic RNAs) (Sun et al., 2013), whereas another is COLDAIR (coldassisted intronic noncoding RNAs), which is transcribed in sense orientation from the intron of FLC gene (Liu et al., 2010). Both lncRNAs promote PHD-PRC2 to protein modification. FLC is a key regulator of flowering time as Michaels and Amasino (1999) reported that in A. thaliana FLC acts as a repressor that negatively regulate the floral induction under cold temperature.

17.8 Role of sRNAs in the development of leaf and leaf size and morphology Shoot apical meristem is the peripheral region from where leaves are formed as well as their adaxial
abaxial polarity is determined. In adaxial side, two gene HD-ZIP III genes, PHABULOSA (PHB) and PHA-VOLUTA (PHV), are locally expressed. The adaxial expression of HD-ZIP III genes is basically based on the expression of miRNA165/166, which binds to HD-ZIP III transcripts and degrades the abaxial region (Kidner and Martienssen, 2004). AGO1 is essential for targeting miR165/166 to HD-ZIP III transcripts in leaves and also essential for PHB gene expression. Montgomery (2008) in A. thaliana reported that miR390 is one of the genes that binds to AGO7 and directs the cleavage of precursor ta-siRNAs, which is responsible for promoting growth. A number of miRNAs have been actively involved in the floral organization, as the petal shape and size is regulated by miR319
TCP, and alteration in the MIR319a gene diminishes petal length and width (Nag, 2009), anther development in plants also regulated by miR167 that triggers the ARF6 and ARF8 genes (Wu, 2006) (Fig. 17.3). However alterations in both the genes lead to distortion in stamen filament and defective pollen additionally, miR393 is identified to target AUXIN SIGNALING F-BOX genes, which are also involved in floral organization (Parry et al., 2009). Furthermore, miR159 regulates anther development by interacting with MYB33 (Achard, 2004). According to Allen (2007), decreased expression of miR159 caused fertility, stunted anthers, small siliques, and small seeds. Phytohormones such as gibberellin (GA) upregulates the accumulation of miR159, which shows inter relation of miRNAs and hormones in plant development (Fig. 17.3).

17.9 Role of sRNAs in alleviating salt stress Several studies have been reported supporting the fact that sRNAs play significant role in alleviating and mitigating salt stress in plants because when plants are exposed to salt stress, it downregulate the genes for protein laccase-like proteins (LAC) and casein kinase (CKB3) proteins, which are responsible for tolerance, but overexpression of miR397 in transgenic Arabidopsis upregulates the genes for LAC and CKB3 transcript and increases the tolerance behaviors of plants against salt stress. In Oryza sativa, miRNAs from miR169 family, that is, miR169g and miR169n, described as salt-responsive gene were considerably tempted during salt stress, which is responsible for cleavage of a CCAAT-box-binding transcription factor (Zhao, 2009). Similarly in Arabidopsis, miR169 was pointedly induced on exposure to salt stress. Thus miR169 was considered salt-responsive miRNA family (Fig. 17.2). Plant Life under Changing Environment

475

17.10 Role of sRNAs in oxidative stress regulation

A RN

Coding sequence

mRNAs

Noncoding sequence

Oxidative stress

Activation of miRNAs 198

rRNAs

CSD-2

miRNAs siRNAs tasiRNAs

rasiRNAs

Membrane damage and disturbs the membrane integrity

Reduce pigment content and photosynthetic rate

Reduced growth

Activation of transcript

sRNA

CSD-1

tRNAs

Abiotic responses in plants

Increased generation of ROS

ants in pl A of N R sion c of m pres h abioti x e Role and ed wit n o i ciat ulat Reg ins asso ce e n t a o r e pr s tol stres Abiotic tolerance

Deactivation of ROS

sRNAs synthesis and mobility

Chlorophyllase enzyme Degradation of α-aminolevulinic dehydrogenase responsible for chlorophyll synthesis Resistance to stress

sRNAs are mobile and mobility is through cell to cell, that is, through plasmodesmata, generated sRNAs move long distance, root to shoot, by a repeating cell-to-cell mechanism

Poor yield

FIGURE 17.3 Role of sRNA in plants in response to various abiotic stresses.

17.10 Role of sRNAs in oxidative stress regulation Oxidative stress is a multifaceted biochemical phenomenon that convoys various biotic and abiotic stresses and develops as a result of accumulation and overproduction of reactive oxygen species (ROS). ROS, i.e., super oxide radicle (SOR), O2•2 and H2O2, it is widely believed that “electron leakage” in electron transport chains of chloroplasts and mitochondria is the major contributor (Devert et al., 2015). The function of superoxide dismutase (SOD) in plants is to scavenge the SOR and convert it into in O2 and H2O2. The two forms of SOD, that is, Cu/Zn SOD, are formed due to expression of genes such as cytosolic CSD1 and plastidic CSD2, and both are targeted by miR398 (Khraiwesh et al., 2012). Overexpression of (Cu/Zn-SODs) superoxide dismutase which scavenges superoxide radicals (Sunkar et al., 2006). Sunkar et al. (2006) presented a better approach to resolve this problem by overexpressing miR398-resistant form of CSD2, which led to increased tolerance to high-intensity light, heavy metals, and other oxidative stresses, and cleavages of both the CSD1 and CSD2 transcripts were mediated by miR398 (Jones-Rhoades and Bartel, 2004). In Arabidopsis plant, three loci, namely MIR398a, MIR398b, and MIR398c, are part of the miR398 family (Bonnet et al., 2004). Under oxidative stress conditions the expression of miR398is downregulated, which results in posttranscriptional accumulation of SOD genes, namely CSD1 and CSD2 mRNA (formed by miR398-directed mRNA cleavage) and participates in stress tolerance (Sunkar et al., 2006). Furthermore, transgenic Arabidopsis under high light, heavy metals, and other oxidative stressors showed overexpressing CSD2 mRNA that mediates the stress tolerance (Fig. 17.2).

Plant Life under Changing Environment

476

17. Role of sRNAs in abiotic stress tolerance

17.11 Role of sRNAs in signaling of hormone sRNAs are also endeavored to act as hormone modulator as expression of miR393, which targets the auxin binding with F-box auxin receptor genes, including transport inhibitor response 1 (TIR1), which, in turn, targets AUX/IAA proteins by SCF E3 leads to the ubiquitylation that necessary for auxin responses and results in growth and development (Vierstra, 2003; Fig. 17.3). However, stressful environment leads to the downregulation of TIR1, which degrades the synthesis of mRNA or represses the translational process (Sunkar and Zhu, 2004). This TIR1 leads to the downregulation of auxin signaling, which affects the plant and seedling growth (Navarro et al., 2006). Moreover, there is a gap of lacking the hypothesis to show the link of plant/pathogen responses and auxin synthesis by miR393.

17.12 Conclusion Around the world, various biotic as well as abiotic stresses limit the crop productivity due to imbalance in physiological, biochemical, and molecular responses under abiotic factors, which include reduction in photosynthetic pigments associated with loss in wholecell oxygen evolution, that is, photosynthesis. Therefore the gross primary productivity of crop is reduced. Besides this, abiotic factors also contribute to oxidative stress by generating ROS and subsequently damaged the macromolecules such as proteins, lipids, and DNA. To mitigate the adverse effects, plants modifies its physiological attributes at molecular level by down- or upregulating the gene expression responsible for particular protein expression. In plant development, sRNA acts as key regulators and significantly involve in abiotic stress tolerance. In general, sRNA divided into two forms, miRNA and siRNA, which actively mediate the gene silencing termed RNAi. It is the mechanism that inhibits the gene expression at transcriptional and posttranslational level by the involvement of Dicer and binds with mRNA via dsRNA-enzyme complex named AGO protein and leads to the degradation of mRNA strand. RNA interference is a defensive mechanism against stress tolerance as well as against pathogens and also allows agricultural benefits in crop species.

References Achard, P., 2004. Modulation of floral development by a gibberellin-regulated microRNA. Development 131, 3357
3365. Ahmad, P., Hakeem, K.R., Kumar, A., Ashraf, M., Akram, N.A., 2012. Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). Afr. J. Biotechnol. 11, 2694
2703. Allen, R.S., 2007. Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc. Natl. Acad. Sci. U.S.A. 104, 16371
16376. Allen, E., Xie, Z., Gustafson, A.M., Sung, G.H., Spatafora, J.W., Carrington, J.C., 2004. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 36, 1282
1290. Barakat, A., Sriram, A., Park, J., Zhebentyayeva, T., Main, D., Abbott, A., 2012. Genome wide identification of chilling responsive microRNAs in Prunus persica. BMC Genomics 13, 481.

Plant Life under Changing Environment

References

477

Bartel, B., Bartel, D.P., 2003. MicroRNAs: at the root of plant development? Plant Physiol. 132, 709
717. Baulcombe, D., 2000. Unwinding RNA silencing. Science 290, 1108
1109. Baulcombe, D., 2004. RNA silencing in plants. Nature 431, 356
363. Bonnet, E., Wuyts, J., Rouze, P., Van de Peer, Y., 2004. Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc. Natl. Acad. Sci. U.S.A. 101, 11511
11516. Bortolamiol, D., Pazhouhandeh, M., Marrocco, K., Genschik, P., Ziegler-Graff, V., 2007. The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 17, 1615
1621. Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y., et al., 2010. Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLoS One 5, 9514. Burkhart, K.B., Guang, S., Buckley, B.A., Wong, L., Bochner, A.F., Kennedy, S., 2011. A pre-mRNA-associating factor links endogenous siRNAs to chromatin regulation. PLoS Genet. 7, 1002249. Carrington, J.C., Ambros, V., 2003. Role of micro RNAs in plant and animal development. Science 301, 336
338. Carthew, R.W., Sontheimer, E.J., 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642
655. Dalmay, T., Hamilton, A., Mueller, E., Baulcombe, D.C., 2000. Potato virus X amplicons in Arabidopsis mediate genetic and epigenetic gene silencing. Plant Cell 12, 369
379. Devert, A., Fabre, N., Floris, M., Canard, B., Robaglia, C., Cre´te´, P., 2015. Primer-dependent and primerindependent initiation of double stranded RNA synthesis by purified Arabidopsis RNA-dependent RNA polymerases RDR2 and RDR6. PLoS One 10, 0120100. Ding, J., Lu, Q., Ouyang, Y., Mao, H., Zhang, P., Yao, J., 2012. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Natl. Acad. Sci. U.S.A. 109, 2654
2659. Fahlgren, N., Howell, M.D., Kasschau, K.D., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., et al., 2007. Highthroughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of miRNA genes. PLoS One 2 (2), e219. Available from: https://doi.org/10.1371/journal.pone.0000219. Gasciolli, V., Mallory, A.C., Bartel, D.P., Vaucheret, H., 2005. Partially redundant functions of Arabidopsis dicerlike enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15, 1494
1500. Gehan, M.A., Greenham, K., Mockler, T.C., McClung, C.R., 2015. Transcriptional networks—crops, clocks, and abiotic stress. Curr. Opin. Plant Biol. 24, 39
46. Grime, J.P., 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111, 1169
1194. He, Y., 2012. Chromatin regulation of flowering. Trends Plant Sci. 17, 556
562. Held, M.A., Penning, B., Brandt, A.S., Kessans, S.A., Yong, W., Scofield, S.R., 2008. Small-interfering RNAs from natural antisense transcripts derived from a cellulose synthase gene modulate cell wall biosynthesis in barley. Proc. Natl. Acad. Sci. U.S.A. 105, 20534
20539. Heo, J.B., Sung, S., 2011a. Encoding memory of winter by noncoding RNAs. Epigenetics 6, 544
547. Heo, J.B., Sung, S., 2011b. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76
79. Herr, A.J., 2005. RNA polymerase IV directs silencing of endogenous DNA. Science 308, 118
120. Hilbricht, T., 2008. Retro transposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytol. 179, 877
887. Huang, J., Yang, M., Lu, L., Zhang, X., 2016. Diverse functions of small RNAs in different plant
pathogen communications. Front. Microbiol. 7, 1552. Hutvagner, G., Mlynarova, L., Nap, J.P., 2000. Detailed characterization of the post transcriptional gene-silencingrelated small RNA in a GUS gene-silenced tobacco. RNA Soc. 6, 1445
1454. Islam, W., Islam, Su, Qasim, M., Wang, L., 2017. Host
Pathogen interactions modulated by small RNAs. RNA Biol. 14, 891
904. Jones-Rhoades, M.W., Bartel, D.P., 2004. Computational identification of plant micro RNAs and their targets, including a stress-induced miRNA. Mol. Cell 14, 787
799. Kamthan, A., Chaudhuri, A., Kamthan, M., Datta, A., 2015. Small RNAs in plants: recent development and application for crop improvement. Front. Plant Sci. 6, 208. Khraiwesh, B., Zhu, J.K., Zhu, J., 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta. 1819, 137
148.

Plant Life under Changing Environment

478

17. Role of sRNAs in abiotic stress tolerance

Kidner, C.A., Martienssen, R.A., 2004. Spatially restricted microRNA directs leaf polarity through Argonaute1. Nature 428, 81
84. Kim, V.N., 2005. Small RNAs: classification, biogenesis, and function. Mol. Cell 19, 1
15. Ku, Y.S., Wong, J.W.H., Mui, Z., Liu, X., Hui, J.H.L., Chan, T.F., et al., 2015. Small RNAs in plant responses to abiotic stresses: regulatory roles and study methods. Int. J. Mol. Sci. 16, 24532
24554. Law, J.A., Jacobsen, S.E., 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204
220. Lim, L.P., 2003. The microRNAs of Caenorhabditis elegans. Genes Dev. 17, 991
1008. Lingel, A., Simon, B., Izaurralde, E., Sattler, M., 2004. Nucleic acid 30 -end recognition by the Argonaute. Nat. Struct. Mol. Biol. 11, 576
577. Liu, F., Marquardt, S., Lister, C., Swiezewski, S., Dean, C., 2010. Targeted 30 processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327, 94
97. Mantri, N., Patade, V., Penna, S., Ford, R., Pang, E., 2012. Abiotic stress responses in plants present and future. In: Ahmad, P., Prasad, M.N.V. (Eds.), Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability. Springer, New York, pp. 1
19. Marenkova, T.V., Deineko, E.V., 2010. Transcriptional gene silencing in plants. Russ. J. Genet. 46, 511
520. Matzke, M., Matzke, A., Pruss, G., Vance, V., 2001. RNA-based silencing strategies in plants. Curr. Opin. Genet. Dev. 11, 221
227. Matzke, M., Kanno, T., Daxinger, L., Huettel, B., Matzke, A.J., 2009. RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21, 367
376. Meister, G., 2013. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 14, 447
459. Meister, G., Tuschl, T., 2004. Mechanisms of gene silencing by double-stranded RNA. Nature 431, 343
349. Mette, M., Aufsatz, W., Vander-Winden, J., Matzke, M., Matzke, A., 2000. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 19, 5194
5201. Michaels, S.D., Amasino, R.M., 1999. Flowering locus C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949
956. Moldovan, D., 2010. Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J. Exp. Bot. 61, 165
177. Moldovan, D., Spriggs, A., Yang, J., Pogson, B.J., Dennis, E.S., Wilson, I.W., 2010. Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J. Exp. Bot. 61, 165
177. Montgomery, T.A., 2008. Specificity of Argonaute7—miR390 interaction and dual functionality in TAS3 transacting siRNA formation. Cell 133, 128
141. Nag, A., 2009. miR319 a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106, 22534
22539. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., et al., 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436
439. Nicaise, V., 2014. Crop immunity against viruses: outcomes and future challenges. Front. Plant Sci. 5, 660. Nishimura, T., Molinard, G., Petty, T.J., Broger, L., Gabus, C., Thanos, D., et al., 2012. Structural basis of transcriptional gene silencing mediated by Arabidopsis MOM1. PLoS Genet. 2, 1002484. Noman, A., Aqeel, M., 2017. miRNA-based heavy metal homeostasis and plant growth. Environ. Sci. Pollut. Res. 24, 10068
10082. Noman, A., Aqeel, M., Deng, J., Khalid, N., Sanaullah, T., Shuilin, H., 2017. Biotechnological advancements for improving floral attributes in ornamental plants. Front. Plant Sci. 8, 530. Ouyang, S., Park, G., Atamian, H.S., Han, C.S., Stajich, J.E., Kaloshian, I., et al., 2014. MicroRNAs suppress NB domain genes in tomato that confer resistance to Fusarium oxysporum. PLoS Pathog. 10, 1004464. Parry, G., Calderon-Villalobos, L.I., Prigge, M., Peret, B., Dharmasiri, S., Itoh, H., et al., 2009. Complex regulation of the TIR1/AFB family of auxin receptors. Proc. Natl. Acad. Sci. U.S.A. 106, 22540
22545. Shanker, A.K., Venkateswarlu, B., 2011. Abiotic Stress in Plants—Mechanisms and Adaptations, 9. Tech, Janeza Trdine, p. 51000. Shivaprasad, P.V., Chen, H.M., Patel, K., Bond, D.M., Santos, B.A., Baulcombe, D.C., 2012. A microRNA superfamily regulates nucleotide binding site
leucine-rich repeats and other mRNAs. Plant Cell 24, 859
874. Shukla, L.I., Chinnusamy, V., Sunkar, R., 2008. The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim. Biophys. Acta. 11, 743
748.

Plant Life under Changing Environment

References

479

Singh, M., Singh, V.P., Prasad, S.M., 2016. Nitrogen modifies NaCl toxicity in eggplant seedlings: Assessment of chlorophyll a fluorescence, antioxidative response and proline metabolism. Biocatal. Agric. Biotechnol. 7, 76
86. Singh, R., Parihar, P., Prasad, S.M., 2018. Sulphur and calcium simultaneously regulate photosynthetic performance and nitrogen metabolism status in As challenged Brassica juncea L. seedlings. Front. Plant. Sci. 9, 772. Song, J.J., Liu, J., Tolia, N.H., Schneiderman, J., Smith, S.K., 2003. The crystal structure of the argonaute reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 10, 1026
1032. Song, J.J., Smith, S.K., Hannon, G.J., Joshua-Tor, L., 2004. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305, 1434
1437. Song, Y.H., Ito, S., Imaizumi, T., 2013. Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends. Plant. Sci. 18, 575
583. Sousa, C., Johansson, C., Charon, C., Manyani, H., Sautter, C., Kondorosi, A., 2001. Translational and structural requirements of the early nodulin gene enod40, a short-open reading frame containing RNA, for elicitation of a cell-specific growth response in the alfalfa root cortex. Mol. Cell. Biol. 21, 354
366. Sun, Q.W., Csorba, T., Skourti-Stathaki, K., Proudfoot, N.J., Dean, C., 2013. R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340, 619
621. Sunkar, R., Girke, T., Jain, P.K., Zhu, J.K., 2005. Cloning and characterization of microRNAs from rice. Plant Cell 17, 1397
1411. Sunkar, R., Kapoor, A., Zhu, J.K., 2006. Post transcriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by down regulation of miR398 and important for oxidative stress tolerance. Plant Cell 18, 2051
2065. Sunkar, R., Zhu, J.K., 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16, 2001
2019. Swiezewski, S., Liu, F., Magusin, A., Dean, C., 2009. Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature 462, 799
802. Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M., Watanabe, Y., 2008. The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol. 49, 493
500. Thakur, P., Kumar, S., Malik, J.A., Berger, J.D., Nayyar, H., 2010. Cold stress effects on reproductive development in grain crops: an overview. Environ. Exp. Bot. 67, 429
443. Vaillant, I., Schubert, I., Tourmente, S., Mathieu, O., 2006. MOM1 mediates DNA methylation independent silencing of repetitive sequences in Arabidopsis. EMBO Rep. 7, 1273
1278. Vanyushin, B.F., 2006. DNA methylation and epigenetics. Russ. J. Genet. 42, 1186
1199. Vierstra, R.D., 2003. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant. Sci. 8, 135
142. Wang, H.L.V., Chekanova, J.A., 2016. Small RNAs: essential regulators of gene expression and defenses against environmental stresses in plants. Wiley Interdiscip. Rev. RNA 7, 356
381. Wassenegger, M., Heimes, S., Riedel, L., Sanger, H., 1994. RNA directed de novo methylation of genomic sequences in plants. Cell 76, 567
576. Weiberg, A., Jin, H., 2015. Small RNAs the secret agents in the plant
pathogen interactions. Curr. Opin. Plant Biol. 26, 87
94. Wroblewski, T., Piskurewicz, U., Tomczak, A., Ochoa, O., Michelmore, R.W., 2007. Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant J. 51, 803
818. Wu, M.F., 2006. Arabidopsis micro-RNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211
4218. Yang, W.C., Katinakis, P., Hendriks, P., Smolders, A., de Vries, F., Spee, J., 1993. Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J. 3, 573
578. Yao, Y., 2010. ). Non-coding small RNAs responsive to abiotic stress in wheat (Triticum aestivum L.). Funct. Integr. Genomics 10, 187
190. Zaynab, M., Kanwal, S., Hussain, I., Qasim, M., Noman, A., Iqbal, U., et al., 2017. Rice chitinase gene expression in genetically engineered potato confers resistance against Fusarium solani and Rhizictonia solani. P.S.M. Microbiol. 2, 63
73.

Plant Life under Changing Environment

480

17. Role of sRNAs in abiotic stress tolerance

Zhang, W., Gao, S., Zhou, X., Chellappan, P., Chen, Z., Zhou, X., et al., 2011. Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol. Biol. 2011 (75), 93
105. Zhao, B., 2009. Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol. Biol. 10, 29. Zhao, H., Sun, R., Albrecht, U., Padmanabhan, C., Wang, A., Coffey, M.D., et al., 2013. Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus huanglongbing disease. Mol. Plant. 6, 301
310. Zheng, B., Wang, Z., Li, S., Yu, B., Liu, J.Y., Chen, X., 2009. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23, 2850
2860. Zubko, E., Meyer, P., 2007. A natural antisense transcript of the Petunia hybrida Sho gene suggests a role for an antisense mechanism in cytokinin regulation. Plant J. 52, 1131
1139. Zvereva, A.S., Pooggin, M.M., 2012. Silencing and innate immunity in plant defense against viral and non-viral pathogens. Viruses 4, 2578
2597.

Further reading Ellendorff, U., Fradin, E.F., de Jonge, R., Thomma, B.P.H.J., 2008. RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 60, 591
602. Gitschier, J., 2013. How cool is that: an interview with Caroline Dean. PLoS Genet. 9, 1003593. Jen, C.H., Michalopoulos, I., Westhead, D.R., Meyer, P., 2005. Natural antisense transcripts with coding capacity in Arabidopsis may have a regulatory role that is not linked to double-stranded RNA degradation. Genome Biol. 6, 51. Katiyar-Agarwal, S., Jin, H., 2010. Role of small RNAs in host-microbe interactions. Annu. Rev. Phytopathol. 48, 225
246. Katiyar-Agarwal, S., Gao, S., Vivian-Smith, A., Jin, H., 2007. A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev. 21, 3123
3134. Kooter, J.M., Matzke, M.A., Meyer, P., 1999. Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci. 4, 340
347. Kutter, C., Schob, H., Meins Jr., F., Si-Ammour, A., 2007. MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19, 2417
2429. Mette, M.F., Vander-Winden, J., Matzke, M., Matzke, A.J., 2002. Short RNAs can identify new candidate transposable element families in Arabidopsis. Plant Physiol. 130, 6
9. Song, J., Angel, A., Howard, M., Dean, C., 2012. Vernalization a cold induced epigenetic switch. J. Cell. Sci. 125, 3723
3731. Vadim, D., 2015. Review mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ. Exp. Bot. 109, 212
228. Zhou, H., Liu, Q., Li, J., Jiang, D., Zhou, L., Wu, P., 2012. Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 22, 649
660.

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C H A P T E R

18 Role of polyamines in plants abiotic stress tolerance: Advances and future prospects Chanda Bano, Nimisha Amist and N.B. Singh Plant Physiology Laboratory, Department of Botany, University of Allahabad, Prayagraj, India

18.1 Introduction Plants face a variety of environmental stresses due to their sessile nature and encounter several stresses throughout the life cycle. Environmental stresses negatively affect the development and productivity of plants (Tuteja, 2009). During the last decade, in different parts of the world, environmental stresses such as drought, salt, cold, and UV have affected agricultural land (Mahajan and Tuteja, 2005; Rengasamy, 2006). Different stresses hamper crop cultivation and yield, and due to abiotic stresses, each year many countries lose significant money from decrement in yield of crop (Mahajan and Tuteja, 2005). In response to climate change, abiotic stresses become more severe and frequent, particularly in response to global warming. In addition, the hastily increasing world population, estimated to reach near 10 billion by 2050, consequently causes severe food scarcity. Consequently, to give food to the burgeoning population, tolerant crops should be developed. Polyamines (PAs) are present in all living organisms, and at physiological pH, they are positively charged. These are small, organic molecules that are ubiquitously present in all living organisms and regarded as growth substance. In plants, commonly present PAs are putrescine (Put), spermidine (Spd), and spermine (Spm). Thermospermine (tSpm) in place of or in addition to Spm is present in some plants. They are simple in their structure, present in all parts of the cell, and involved in physiological activities ranging from structural stabilization of key macromolecules to cellular membranes to make them an attractive group of metabolites to allot a large number of natural functions. Plants have PAs in different forms such as free, soluble conjugated, and insoluble bound (Lefevre et al., 2001). They are soluble and covalently conjugated to molecules, namely phenolic compounds, while macromolecules such as nucleic acids and proteins are bound to insoluble PAs Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00021-7

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covalently (Duan et al., 2008). In a large number of biological systems, such as plants, animals, algae, and bacteria, some uncommon PAs, such as homospermidine, 1,3-diaminopropane (DAP), cadaverine, and canavalmine, have been detected. Polycationic nature of PAs is a remarkable feature that plays a significant function in their biological activities (Valero et al., 2002). In cell PAs accretion in large quantity most probably seize extra nitrogen (N), thus decreasing ammonia toxicity, and also balance the total N allocation into several pathways. Imbalance in their concentration is related to the responses of plants against various stresses and different phases of growth too which is not surprising. They prepare plant to overcome varied stress condition, and their catabolic products are responsible for causing stress damage. The interaction between PAs and abiotic stress in plants and their apparently contradictory roles in the process have been documented over the years (Galston and Sawhney, 1990; Alca´zar et al., 2011; Kusano et al., 2007; Liu et al., 2007; Bachrach, 2010; Alet et al., 2011; Hussain et al., 2011; Shi and Chan, 2014). The major challenge faced by modern agriculture is maintaining crop production under environmental stresses. Plants have efficient defense mechanisms to overcome environmental stresses (Fujita et al., 2006). PAs act as stress messengers in plant responses to stress signals (Liu et al., 2000, 2007). PAs also play important roles in defense response of plants to several environmental stresses (Bouchereau et al., 1999), including metal toxicity (Groppa et al., 2003), oxidative stress (Rider et al., 2007), drought (Yamaguchi et al., 2007), salinity (Duan et al., 2008), and chilling stress (Cuevas et al., 2008; Groppa and Benavides, 2008). The previous report supported that PAs application increases stress tolerance and productivity of crop. It has been reported that the application of Put is used to increase salinity (Chattopadhayay et al., 2002; Verma and Mishra, 2005; Ndayiragije and Lutts, 2006), cold (Nayyar and Chander, 2004; Nayyar, 2005), drought (Zeid and Shedeed, 2006), heavy metals (Wang et al., 2007), osmotic stress (Liu et al., 2006), high temperature, (Murkowski, 2001), water logging (Arbona et al., 2008), and flood tolerance in plants (Yiu et al., 2009). Genetic change in genes encoding arginine decarboxylase (ADC), ornithine decarboxylase (ODC), S-adenosylmethionine decarboxylase (SAMDC), or Spd synthase (SPDS) enhanced tolerance against abiotic stress (Liu et al., 2007). It is fascinating to note that genetically modified plants can endure stress conditions such as toxicity of parquet, drought, low and high temperature, and salinity. In this chapter, we have tried to summarize the information that has been reported over the last couple of decades concerning the changes in metabolism of PA under different abiotic stress.

18.2 Synthesis of polyamines under abiotic stresses PAs are present in all plant cells. PAs are a group of aliphatic amine compounds. PAs include diamine Put [NH2(CH2)4NH2], triamine Spd [NH2(CH2)3NH(CH2)4NH2], and tetramine Spm [NH2(CH2)3NH(CH2)4NH(CH2)3NH2]. PAs synthesis and their catabolism in plants are well represented in PAs biosynthesis pathway. The number of positive charges on PAs differs in the cell at different physiological pH. The production of Put is either from decarboxylation of the amino acid L-ornithine by ODC (EC 4.1.1.17) or by the decarboxylation of L-arginine by ADC (EC 4.1.1.19) via agmatine (Slocum, 1991). In response of

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Metheonine

Arginine

9

1 N-Carbamoylputrescine

S-Adenosylmethionine (SAM)

2

11

Acetyl-CoA carboxylase (ACC)

12 Ethylene

10 Decarboxylated S-Adeosylmethionine (dcSAM)

Agmatine 3 6 Ornithine

Spermine

Spermidine

Putrescine 7 4 Δ-Pyrroline 5 Δ-Aminobutyric acid

8 1. Arginine decarboxylase (ADC) 2. N-Carbamoylputrescine amidohydrolase (CPA) 3. Agmatine deiminase (ADI) 4. Diamine oxidase (DAO) 5. Δ-Pyrroline dehydrogenase 6. Ornithine decarboxylase (ODC) 7. Spermidine synthase (SPDS) 8. Spermine synthase (SPMS) 9. S-Adenosylmethionine synthase 10. S-Adenosylmethionine decarboxylase (SAMDC) 11. 1-Aminocyclopropane-1-carboxylic acid synthase 12. 1-Aminocyclopropane-1-carboxylic acid oxidase

FIGURE 18.1 Diagrammatic representation of polyamines biosynthetic pathway. Source: Modified from Gill, S.S., Tuteja, N., 2010. Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 51, 26
33.

different stresses, PAs synthesis is induced by the ADC pathway (Bouchereau et al., 1999; Kuznetsov and Shevyakova, 2007). During the initial stage of plant growth, development, organ differentiation, and reproductive stage, ODC pathway is more active. Spd and Spm are formed by the successive attachment of aminopropyl with Put which will initially synthesize Spd, and then Spd will synthesize spermine (Spm) (Slocum, 1991; Knott et al., 2007). The production of Spd by SPDS via addition to Put of an aminopropyl moiety came from decarboxylated S-adenosylmethionine produced by SAMDC. In ADC production, agmatine is converted into Put via an intermediate N-carbamoylputrescine. Conversion of agmatine in Put involves two separate enzymes: N-carbamoylputrescine amidohydrolase (CPA) and agmatine deiminase. In the production of higher PA Spm, Spd acts as a substrate. Diamine oxidases (DAOs) catabolize Put, that changes Put into Δ1-pyrroline, and form ammonia and H2O2 as by-products. Further, Δ1-pyrroline is degraded into γ-aminobutyric acid as shown in Fig. 18.1, which is ultimately changed into succinic acid (Krebs cycle component) (Eller et al., 2006). This chapter concluded that the PAs play a constructive role in abiotic stress tolerance. The level of free PAs is maintained during normal and stress conditions by PA catabolic pathways (Martin-Tanguy, 2001; Paschalidis and Roubelakis-Angelakis, 2005).

18.3 Metabolism of polyamine during different stress conditions A few decades ago, the role of PA during abiotic stress tolerance came under intense search after an augment in Put due to K1 scarcity. Several researches have been performed Plant Life under Changing Environment

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to investigate amendment in PA, when plants are exposed to individual or combined stresses (Urano et al., 2003; Kuthanova´ et al., 2004; Liu et al., 2006). PA-formation pathway and involved enzymes are under intricate metabolic and developmental control, and such control is obligatory for well-organized cell metabolism. ADC (ADC1 and ADC2) differential expression has been observed in Arabidopsis, under stress situation. Environmental stresses such as drought, high salinity, mechanical injury, and potassium (P) scarcity powerfully induced ADC2 expression (Pere´z-Amador et al., 2002; Urano et al., 2003; Armengaud et al., 2004; Hummel et al., 2004; Alca´zar et al., 2006), whereas ADC1 is mostly activated by cold (Hummel et al., 2004). Likewise, the expression of SPMS and ADC2 follows the same pattern in PA accretion during dehydration and high salinity (Urano et al., 2003; Alca´zar et al., 2006). On the other hand, during different stresses, SPDS2 has constitutive expression opposite to SPDS1 that exhibits enhanced expression under dehydration. Similarly, the expression of both SAMDC1 and SAMDC2 are activated by cold, and SAMDC2 has slight activation in expression in salt-stress response (Vergnolle et al., 2005). None of these stresses have the capability to affect the CPA, agmatine iminohydrolase (AIH), and ACL5 expression patterns (Alca´zar et al., 2006). At transcriptional, translational, and posttranslational levels of PA formation, enzymes (ODC, ADC, and SAMDC) are controlled (Hu et al., 2005); these PA biosynthesis enzymes are primarily synthesized as an inactive precursor (proenzyme), ultimately by posttranslational processing becoming mature enzymes (Xiong et al., 1997). During environmental fluctuations, Put accretion has been observed concomitant with ADC2 and ADC1 upregulation. On the other hand, accretion and activation of Put downstream genes are implicated in the formation of Spd and Spm (SAMDC2, SPDS1, and SPMS), which did not influence the both PAs content. Translational or posttranslational products of SAM decarboxylase are significant for the formation of PA. Hu et al. (2005) also observed that 50 -untranslated sequence plays a central role in transcriptional and posttranscriptional control of SAMDC gene expression. During stress, the level of PA could also be regulated by its catabolism. Catabolic pathway controlling PA (Bagni and Tassoni, 2001; Cona et al., 2006) involves two amine oxidases, DAO and PA oxidase (PAO). Put is changed into pyrroline, ammonia, and H2O2 by DAO. Spd by PAO to pyrroline, DAP, H2O2 and Spm to aminopropylpyrroline, DAP and H2O2 (Martin-Tanguy, 2001; Sebela et al., 2001; Cona et al., 2003, 2006). High concentration of Spd and Spm was produced by rice 3 days after drought stress, but the level showed reduction abruptly after 6 days, probably because of the action of PAO (Capell et al., 2004). ABA level showed enhancement in response to stresses (Christmann et al., 2005). Expression of number of genes participating in stress tolerance is activated by ABA (Yamaguchi et al., 2007). ABA activates genes that participate in the formation of PA (Alca´zar et al., 2006). The expression of ADC2, SPDS1, and SPMS due to dehydration is an ABA-dependent response because activation of these genes is not observed in ABA scarce (aba2) and insensitive (abi1) mutants (Alca´zar et al., 2006). Furthermore, it is revealed that ABA responsive (ABRE and/ or ABRE-related motifs) and stress elements (DRE and LTR) are present in these gene promoters site. Microarray analysis has demonstrated that genes involved in metabolism of PA ¨ ztu¨rk in Arabidopsis activate in response to a variety of abiotic stresses such as drought (O et al., 2002), wounding or methyl jasmonate treatment (Sasaki et al., 2001; Pere´z-Amador et al., 2002). However, microarray technology used for unraveling molecular mechanisms underlying PA effects on abiotic stress tolerance is in its infancy.

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18.4 Polyamines and abiotic stress tolerance in plants PAs participate in the maintenance of normal cellular processes, including DNA replication, transcription, translation, cell production, inflection of enzyme activities, cellular cation
anion balance, and membrane integrity. PAs play chief function in a variety of growth and developmental processes such as cell division, dormancy breaking of tubers and germination of seeds, development of flower buds, embryogenesis, fruit set and growth, fruit maturation, morphogenesis and response to stresses (Bouchereau et al., 1999; Groppa and Benavides, 2008). PAs also participate in the acquisition of endurance to stresses such as elevated and low temperatures, salinity, hyperosmosis, low oxygen, and environmental pollutants (Liu et al., 2007; Garcıa-Jimenez et al., 2007). Salinity impact on growth, ethylene formation, and concentration of PA in Spinacia oleracea, Lactuca sativa, Cucumis melo, Capsicum annuum, Brassica oleracea, Beta vulgaris, and Lycopersicon esculentum is observed by Zapata et al. (2004). PA concentration is altered under salinity stress, and in nearly all cases, Put level is reduced, whereas Spd and/or Spm level is improved (Zapata et al., 2004). Endurance against salinity stress reported might be due to augmented (Spd 1 Spm)/Put ratio. Various plants under salinity stress generate similar response of PAs production. However, varied responses are elicited in plants for ethylene production under salinity stress. In leaves of Triticum aestivum drought-tolerant cv., Yumai No. 18 PEG 6000 treatment increased the free Spd and Spm levels (Liu et al., 2004), whereas increased free Put level is observed in drought-sensitive Yangmai No. 9 cv. Higher ratio of free (Spd 1 Spm)/free Put is observed in Yumai No. 18 cv. than Yangmai No. 9 cv. under osmotic stress. Free Spd, Spm, and PIS-bound Put facilitated the osmotic stress endurance of wheat. Hyposaline shock increased free Put, Spd and Spm, due to a reduced TGase activity, along with an evident increase in the PAs formation that depends on L-arginine (Garcıa-Jimenez et al., 2007). Di and PA (Spd and Spm) steadily acclimated to escalating concentrations (up to 20%, w/v) of polyethylene glycol (PEG 8000). They observed that with respect to di- and PAs, increased tolerance to low-water potential in potato cells leads changes in biosynthesis and conjugation of Put concerned with cell tolerance. In Arabidopsis, AtADC2 is activated under salt stress; consequently, putrescine content is increased that helps in salt-stress endurance. AtADC2 gene is responsible for Put production. Reactive oxygen species (ROS) production increase under salt stress in Cucumis sativus cv. Jinchun No. 2 roots, while activities of antioxidant enzyme and contents of proline were higher in cv. Changchun mici than in cv. Jinchun No. 2 root (Duan et al., 2008). Noticeable elevation in free Spd and Spm, and soluble conjugated and insoluble bound Put, Spd and Spm contents as well as ADO, ODC, SAMDC, and DAO activities under salt stress is observed in the roots Changchun mici than Jinchun No. 2. At low temperature under normal light conditions in winter wheat Mv Emese the level of Put, Spd, and cadaverine is enhanced, whereas in the spring wheat Nadro only Spd and Spm content is increased (Szalai et al., 2009). Nitrate application modulates Put, Spd, and Spm level and production of ethylene in wheat plants grown with ammonia (Garnica et al., 2009). Accretion of PA in Nicotiana tabacum leaves and roots under short-term boron scarcity resulted in declined plant growth (Camacho-Cristobal et al., 2005). During boron scarcity, Put and Spd concentrations in leaves were similar in both treatments, however, in roots, increase in free Put level was observed. Application of S-methylmethionine (SMM)

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maintains cell-membrane integrity, and thus the electrolyte leakage under lowtemperature stress in the leaves and roots of peas, maize, soybeans, and 8-winter wheats (Racz et al., 2008). SMM and PA biosynthesis interaction revealed that level of Agm, Spd, and Put was elevated by SMM, whereas no effect on Spm level was noticed. Varied concentration of Put, Spm, and Spd was observed at different stages of dormancy; at the initial stage of dormancy, an increase in Put and a reduction in Spm and Spd was noticed, whereas Spm and Spd were elevated during dormancy break (Sood and Nagar, 2005). Put amplifies light-energy consumption through photophosphorylation induction (Ioannidis et al., 2006). Put has been reported as a competent stimulator of ATP synthesis when compared to Spd and Spm, but for nonphotochemical quenching, Spd and Spm are efficient stimulators (Ioannidis and Kotzabasis, 2007). In fact, Spd and Spm at high level behave as proficient uncouplers of photophosphorylation. Put and Spm control the size of LHCII, which affected by the low temperate, therefore, amend the structure and function of the chloroplast (Sfakianaki et al., 2006). The declined Put/Spm ratio maybe due to the decreased level of LHCII-associated Put, thus causing amplification of the LHCII. Alterations in the photosynthetic apparatus structure in combination with the reduced photosynthetic electron transfer rate resulted in the inactivation of active reaction centers, and the enhanced dissipated energy diminished the efficiency and rate of photosynthesis. The effect of Calcium nitrate (Ca(NO3)) on the PA contents in leaves of grafted and nongrafted Solanum melongena seedling was studied (Wei et al., 2009). Significant enhanced antioxidant enzymes, namely superoxide dismutase, guaiacol peroxidase, ascorbate peroxidase, and glutathione reductase activities observed in grafted seedlings than those of nongrafted seedlings. Thus they hypothesized the synergistic relationship among antioxidant enzymes and PAs, which contribute toward protective mechanism of grafted eggplant seedlings under Ca(NO3) stress. Rodrıguez-Kessler et al. (2008) reported altered metabolism of PA in maize due the effect of biotrophic pathogenic fungus Ustilago maydis.

18.5 Polyamine accumulating transgenic plants with improved abiotic stress tolerance Modification in PA levels along with role of PA in plant tolerance against stresses has been analyzed through genetic studies. In several plants, alternation of the PA level that led to enhanced plant tolerance against multiple environmental stresses is listed in Table 18.1. Oat ADC mRNA accumulation, increased activity of ADC, and PAs accumulation at diverse levels were observed in tobacco, rice, eggplant, and wheat (Bassie et al., 2008; Moschou et al., 2008). Increased levels of Put, Spd, and Spm induced tolerance in transgenic plants against drought and salt stress. The constitutive (maize ubiquitin 1) and inducible (tetracycline and ABA) promoters were used through the expression of ADC gene obtained from oats and datura for the production of transgenic plants (Capell et al., 2004; Bassie et al., 2008). Put accumulation as well as increased tolerance to dehydration, freezing, and salt stress was observed in transgenic Arabidopsis thaliana (Alet et al., 2011). Elevated synthesis of Put as a result of overexpression of Poncirus trifoliata (PtADC) ADC resulted into enhanced tolerance toward osmotic stresses in A. thaliana (Wang et al., 2011). SAMDC is one of the key enzymes in the biosynthesis of PAs, and to evaluate the impact

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TABLE 18.1 Transgenic plants engineered to encoding polyamine (Put, Spd, and Spm) biosynthetic genes for improved tolerance against abiotic stress. Polyamines genes name

Source organisms

Transgenic plants

Polyamines accumulated

Tolerance developed to stresses

ADC

Avena sativa Datura stramonium A. sativa A. sativa A. sativa Poncirus trifoliata

Oryza sativa O. sativa Solanum melongena Triticum aestivum Arabidopsis thaliana A. thaliana

Putrescine Putrescine, spermidin, Spermine Putrescine, spermidin, spermine Putrescine, spermidin, spermine Putrescine Putrescine

Salinity stress Drought stress Salinity, drought, low and high temperature, and heavy-metal stress Drought stress Drought and freezing stresses Osmotic, drought, cold, and oxidative stresses

ADC2

A. thaliana

A. thaliana

Putrescine

Drought stress

Anti-ACC

Dianthus caryophyllus

Nicotiana tabacum

Spermidin, spermine

Oxidative stress

ODC

Mus musculus

N. tobacum

Putrescine

Salt stress

SAMDC

Hordeum chilense 3 Triticum turgidum Homo sapiens D. caryophyllus Dianthus stramonium Saccharomyces cerevisiae Malus domestica

O. sativa N. tobacum N. tobacum O. sativa Solanum lycopersicum N. tobacum

Spermidin, spermine Putrescine, spermidin Spermidin Spermidin, spermine Spermidin, spermine Spermidin

Salt stress Salt, drought stresses, and fungal wilt Salt, cold, acidic, and oxidative stresses Drought stress Heat and oxidative stresses Frost, salt, and osmotic stresses

SPDS1

Cucurbita ficifolia C. ficifolia M. domestica M. domestica

A. thaliana Ipomoea batatas Pyrus communis P. communis

Spermidin Spermidin Spermidin, spermine Spermidin

Frost, salt, and drought stresses Salt and drought stresses Salt and osmotic stresses Heavy metals and oxidative stresses

ADC, Arginine decarboxylase; ODC, ornithine decarboxylase; SAMDC, S-adenosylmethionine decarboxylase; SPDS, Spd synthase. Adapted from Pathak, M.R., da Silva J.A.T., Wani, S.H., 2014. Polyamines in response to abiotic stress tolerance through transgenic approaches. GM Crops Food 5 (2), 87
96 (Pathak et al., 2014).

of PA biosynthesis on the tolerance of plants against different types of stress, SAMDC gene from different sources was introduced by Agrobacterium tumefaciens and obtained transgenic plants showed superior level of tolerance toward environmental stress and with higher accumulation of PAs than nontransgenic plants (Cheng et al., 2009; Wi et al., 2006). Different SAMDC transgenes of tritordeum (Hordeum chilense 3 Triticum turgidum), carnation (Dianthus caryophyllus), and yeast (Saccharomyces cerevisiae) showed an inducible and constitutive type of expression in response to diverse stresses. SAMDC gene of yeast, Plant Life under Changing Environment

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when expressed constitutively in transgenic tomato plants, accumulated higher levels of Spd and Spm under temperature stress in comparison to wild-type plants and induced tolerance by enhancing antioxidant enzymes activity and lower level of lipid peroxidation in membrane (Cheng et al., 2009). Tobacco plants, transformed with antisense ACC synthase or ACC oxidase from carnation, expressed higher activity of SAMDC and elevated Put and Spd levels as well as tolerance to oxidative stress, high salinity, and low pH (Wi and Park, 2002). Constitutive overexpression of carnation SAMDC and mustard SAMDC in tobacco and A. thaliana, respectively, resulted in the increased level of PAs and produced broad spectrum tolerance to abiotic stresses (Hu et al., 2005; Wi et al., 2006). The SPDS gene’s overexpression in thale cress (A. thaliana), sweet potato (Ipomoea batatas), and pear (Pyrus communis) transgenic cell lines showed an enhanced titer of Spd as well as enhanced tolerance to several abiotic stresses over nontransgenic plants (Kasukabe et al., 2006; Wen et al., 2008). A. thaliana, overexpressing the SPDS cDNA from melon (Cucurbita ficifolia), exhibited a considerable elevation in activity of SPDS along with increased level of Put, Spd, and Spm inducing tolerance to chilling, freezing, salinity, hyperosmosis, and drought (Kasukabe et al., 2004). Furthermore, overexpression of SPDS in transgenic A. thaliana caused increase in expression of various stress-induced transcription factors such as DREB1A, DREB1B, DREB2B along with stress-protective proteins rd29A (Kasukabe et al., 2004). The elevated expression of apple SPDS genes in pear changed PA levels and ultimately enhanced tolerance to multiple abiotic stresses (Wen et al., 2010). Analysis of functional stress-tolerance genes identified the role of PAs and proline as molecular chaperones and also as key-shielding elements in drought, salinity, and temperature stress tolerance (Alet et al., 2012). In the last decade, the awareness about the molecularmechanism-controlling plant’s response to abiotic stresses has improved greatly, and it has been established that a connection exists between protective mechanisms and metabolic networks involved in different processes concerned with stress tolerance. Several abiotic stresses in plant are frequently acknowledged to amend osmotic potential and cause accretion of ROS, whereas PAs may act as regulators of osmotic potential and scavengers of ROS by overexpression of ADC in transgenic A. thaliana (Wang et al., 2011). Induction of nitric oxide (NO) along with overexpression of rat nitric oxide synthase (NOS) occurred in transgenic A. thaliana in response to exogenous application of PAs (Put, Spd, and Spm) and consequently increased tolerance to dehydration stress over nontransgenic plants (Shi and Chan, 2014). Abiotic stress tolerance is an intricate phenomenon that includes the alteration, maintenance, and receptive approach toward stress tolerance in a recurring cross talk by controlling numerous metabolic pathways in which PAs intercede signal transduction (Tiburcio et al., 2012; Cvikrova´ et al., 2013). These observations support the view that enhanced biosynthesis of PA might be an excellent approach in transgenic research in response to plant stress, which also helps in developing tolerance in stresssensitive plants against adverse environmental conditions. PAs play an essential role in increased tolerance to adverse abiotic stresses. On the other hand, inadequate information is available even after overexpression of heterologous genes about the significance of endogenous synthesis of PA along with the activity of endogenous enzymes under salt and drought stresses. Endogenous genes and mutants with decreased activity of enzyme might help to recognize the mechanism of action of metabolism of PA in several stress responses.

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18.6 Polyamines role in response to different abiotic stresses 18.6.1 Metal stress Potassium (K) is an imperative macronutrient and a common stress-related factor carrying essential functions in metabolism of plant, growth, and stress adaptation. The external symptoms of deficiency of metal are more visible on leaves or seedling. Put accretion occurs in the leaves of K-deficient barley (Hordeum vulgare) plants (Richards and Coleman, 1952). Later studies documented that cation
anion equilibrium in plants is maintained due to unambiguous function of Put (Bouchereau et al., 1999). The Put content during K1 deficiency stress is under the directives of ADC activity in A. thaliana (Watson and Malmberg, 1996). Involvement of ADC in Put accretion in bean (Phaseolus vulgaris) seedlings through the use of ADC (DFMA) and ODC enzyme inhibitors (DFMO) under cadmium stress has been established (Weinstein et al., 1986). Afterward, various investigations on the plants subjected to heavy metals, such as Cd, copper (Cu), nickel (Ni), and zinc (Zn), also established the accretion of different PAs and increased activity of ADC (Groppa and Benavides, 2008). The biosynthesis of PA and the antioxidant property of Spm have been correlated to the heavy-metal
stress-tolerance mechanism in plants. Heavy metal stress, such as copper and chromium, elevated the Put and Spd levels in plants that provided them with increased resistance against oxidative damage (Choudhary et al., 2010).

18.6.2 Osmotic, salinity, heat, and/or cold stress Exposure to many osmolyte, such as sorbitol, mannitol, proline, betaine, and sucrose, caused accumulation of Put and Spd in cell and protoplast of oats (Avena sativa) under osmotic stress (Flores and Galston, 1984). ADC transcript level increases under osmotic stress and supports the ADC activation pathway during stress (Borrell et al., 1996). Osmotic stress stimulated an enhancement in the level of Put and diaminopropane (DAP), while a decline occurred in the concentration of Spm in rape (Brassica napus) plants, reflecting the role of Spm in ADC posttranslational regulation. Salinity stimulated PAs accumulation in plants and it appears that their exogenous application assisted rice seedlings in conquering the injurious effects of NaCl (Chattopadhayay et al., 2002). Many studies showed that the exogenous application of different PAs helped to prevail over the stress effect to some extent (Bibi et al., 2010; Yang et al., 2011). Accelerated accumulation of Put and Spd along with increased ADC activity was reported in response to salt and osmotic stress in lupine and apple leaves (Legocka and Kluk, 2005; Liu et al., 2006). Higher level of Spd and Spm was observed in maize seedlings and in flowers and flower stocks of A. thaliana when grown in 200 mM NaCl (Jime´nez-Bremont et al., 2007). The increased levels of Spd and Spm, as well as enhanced expression levels of ADC and SPDS, were recorded in A. thaliana by reverse transcriptase polymerase chain reaction. NaCl stress declined the Spm level in the shoots of Mediterranean salt grass (Aeluropus littoralis), which might be due to the transformation of Spm to higher PAs (Najmeh et al., 2012). A reduction in Put production in PAdeficient mutants of A. thaliana was observed along with lower activity of ADC, resulting into decreased tolerance against salt stress (Kasinathan and Wingler, 2004). Improved

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tolerance against drought in rice might be due to elevated level of bound and free Put (Yang et al., 2007). Elevated level of PAs in barley seedlings regulated the ion channels and maintained K/Na equilibrium eventually increasing the tolerance against stress (Zhao et al., 2007). Exogenous application of PAs caused translocation and accumulation of Put and other PAs in specific organs conferring protection to rice against salt stress (Ndayiragije and Lutts, 2006). Put imparted protection during salt stress in cucumber (C. sativus) by improving water relations and nutrient imbalance (Shu et al., 2012). Heat-tolerant plants showed increased levels of higher PA (Spd and Spm) pools in response to heat stress (Roy and Ghosh, 1996). Special uncommon long-chain PAs, such as norspermidine, norspermine, and caldopentamine, were induced in thermophilic bacterium (Thermus thermophilus) under heat stress (Roy and Ghosh, 1996; Kuehn et al., 1990). In heat-tolerant rice cv “N22,” accumulation of norspermidine and norspermine occurred due to increased activity of ADC and PAO, which was higher than that of heat-sensitive cultivar “IR8.” Exogenous applications of Spd and Spm helped to recover the heat shock in mung bean (Vigna radiata) seedlings (Basra et al., 1997). In rice seedlings, during chilled stress, Spd and Spm contents and SAMDC activity increased (Lee, 1997). In A. thaliana, during heat shock, Put, Spd, and Spm contents are elevated causing the induction of SAMDC2, SPMS, and ADC2 genes. SPMS transgenic plants were protected from heat-shock damage through a similar mechanism as that of exogenously Spm treatment by the expression of heat-shock protein (HPS101, HPS90, and HPS70) genes (Sagor et al., 2013). Impacts of drought stress at most favorable temperatures on free proline and PA levels were observed both in wild and genetically modified soybean seedling for the overproduction of proline (Simon-Sarkadi et al., 2006). In the same way the association of PA and proline in tolerance of drought and heat stress responses in overproduction of proline in transgenic tobacco (N. tabacum) plants. Enhanced Spm level was one factor that imparted tolerance to stress (Cvikrova´ et al., 2013). It appears that proline through its synthesis stimulates tolerance toward stress and indirectly regulates the level of PA. Accumulation of proline and different PAs induced in response to stress were known to improve osmotic stress tolerance and maintain ionic balances in cellular environment (Aziz et al., 1999).

18.7 Polyamine treatment modulated plant-stress tolerance Varied levels of PAs in the cells may, in response to stress, often present clues about the implication of PAs in tolerance against stress, but it doesn’t reveal much evidence about their role in counteracting stress. Detailed information about the biosynthetic pathway of PA and changes taking place due to variations in the pathways can be tested with exogenous PA application/mutant/use of inhibitors of enzymes involved in biosynthetic pathway (Bhatnagar et al., 2002; Alca´zar et al., 2006; Liu et al., 2007). Evidence suggests that exogenous PAs help plant in overcoming stress by maintaining cell-membrane integrity, reducing negative effects on growth, greater expression of genes that involved protection against in osmotic stress, scavenging ROS, maintaining ionic equilibrium, and enhancing antioxidant enzymes activities (Ali, 2000; Iqbal and Ashraf, 2005; Tang and Newton, 2005; Ndayiragije and Lutts, 2006; Afzal et al., 2009; Yiu et al., 2009; Zhang et al., 2009).

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18.8 Conclusion and future perspectives

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However, individual PAs show diverse effect under stress which might be due to differences in absorption, transport, and utilization of PAs among species of plant. Application PA exogenously might activate the genes involved in abiotic stress responses (Gill and Tuteja, 2010). D-Arginine, x-difluoromethylarginine (DFMA), and x-difluoromethylornithine (DFMO) are inhibitors of PA biosynthesis, and their treatment resulted into reduce level of endogenous PA, which further resulted in stress-sensitive phenotypes, but the effect was overturned by application of exogenous PA (He et al., 2002; Navakouidis et al., 2003). However, there is a variation observed in effect of these inhibitors, which depends upon their stability and specificity or on the developmental stage and plant species tested along with competent compensatory mechanisms present in plants (Kaur-Sawhney et al., 2003). An additional genetic approach employed for analyzing PA metabolism and biological functions in stress response is the use of mutants deficient in biosynthesis of PA (Watson et al., 1998; Kaur-Sawhney et al., 2003; Urano et al., 2003). Arabidopsis mutants for ethyl methanesulfonate (EMS) resistance showed decline in ADC activity, spe-1 and spe-2 (Watson et al., 1998) were found to be insufficient in accretion of PA and had reduced tolerance against salt stress in comparison to wild type (Kasinathan and Wingler, 2004). Under normal optimum condition the ADC2 knockout mutant (adc2-1) had no variation in phenotype but was highly vulnerable to salt stress; however, exogenous Put treatment partly alleviates susceptibility toward salt stress (Urano et al., 2003). ADC2 seems to be a main gene, and Put derived from the ADC pathway is an important stress response. Recently, a defective role for Spm in abiotic stresses, such as drought and salinity, was established by the Arabidopsis acl5/spms mutant, defective for Spm production, but this mutant was recovered by application of Spm (Yamaguchi et al., 2006, 2007).

18.8 Conclusion and future perspectives Increased PA biosynthesis, as a result of gene exploitation, is a probable approach to investigate PAs function during abiotic stress and to advance their adaptation to severe environmental situations. Abiotic stresses are the most important cause of crop losses globally, thus employing genetic modification intended to deal with harsh situations. PAs participated in diverse processes including growth, development, and stress tolerance in plants. PA biosynthetic genes engage in tolerance of environmental stress. However, in plants, the function of PAs metabolism in the abiotic stress tolerance is just at the initial stage. A lot of effort is needed to expose the detailed molecular mechanism behind the defensive role of Spd, Spm, and Put in abiotic stress tolerance. Future strategies should use information based on the structure of PA metabolism using PA biosynthetic genes and their regulation by employing diverse types of stress-stimulatory promoters and transcription factors. The sequential study of the genes, encoding the PAs biosynthetic pathways enzymes, will also be helpful in further elevation of the tolerance potentials of crop plants against various stress factors. Furthermore, the external application of PAs can also be subjugated for escalating tolerance against salinity, cold, drought, heavy metal, osmotic stress, high temperature, water logging, and flooding in various crop plants. However, two main areas need further investigation. First, rigorous research at the molecular level is required on signaling function even though strong connection between the presence of PAs and

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improved tolerance toward environmental stresses has been reported. Second, existing information points toward pathogen-stimulated PA synthesis in plants under plant
pathogen interaction. The role of PA in fight against pathogens needs further study. Consequently, researches on PA and stress endurance are at an exciting stage and have created an opening for intensive study to recognize a range of functions of these relatively simple molecules.

References Afzal, I., Munir, F., Ayub, C.M., Basra, S.M.A., Hameed, A., Nawaz, A., 2009. Changes in antioxidant enzymes, germination capacity and vigour of tomato seeds in response of priming with polyamines. Seed Sci. Technol. 37, 765
770. Alca´zar, R., Marco, F., Cuevas, J.C., Patron, M., Ferrando, A., Carrasco, P., et al., 2006. Involvement of polyamines in plant response to abiotic stress. Biotechnol. Lett. 28, 1867
1876. Alca´zar, R., Cuevas, J.C., Planas, J., Zarza, X., Bortolotti, C., Carrasco, P., et al., 2011. Integration of polyamines in the cold acclimation response. Plant Sci. 180, 31
38. Alet, A.I., Sanchez, D.H., Cuevas, J.C., Del Valle, S., Altabella, T., Tiburcio, A.F., et al., 2011. Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signal. Behav. 6, 278
286. Alet, A.I., Sa´nchez, D.H., Cuevas, J.C., Marina, M., Carrasco, P., Altabella, T., et al., 2012. New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Sci. 182, 94
100. Ali, R.M., 2000. Role of putrescine in salt tolerance of Atropa belladonna plant. Plant Sci. 152, 173
179. Arbona, V., Hossain, Z., Lopez-Climent, M.F., Perez-Clemente, R.M., Gomez-Cadenas, A., 2008. Antioxidant enzymatic activity is linked to water logging stress tolerance in citrus. Physiol. Plant 132, 452
466. Armengaud, P., Breitling, R., Amtmann, A., 2004. The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol. 136, 2556
2576. Aziz, A., Martin-Tanguy, J., Larher, F., 1999. Salt stress-induced proline accumulation and changes in tyramine and polyamine levels are linked to ionic adjustment in tomato leaf discs. Plant Sci. 145, 83
91. Bachrach, U., 2010. The early history of polyamine research. Plant Physiol. Biochem. 48, 490
495. Bagni, N., Tassoni, A., 2001. Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20, 301
317. Basra, R.K., Basra, A.S., Malik, C.P., Grover, I.S., 1997. Are polyamines involved in the heat-shock protection of mung bean seedlings? Bot. Bull. Acad. Sin. 38, 165
169. Bassie, L., Zhu, C., Romagosa, I., Christou, P., Capell, T., 2008. Transgenic wheat plants expressing an oat arginine decarboxylase cDNA exhibit increases in polyamine content in vegetative tissue and seeds. Mol. Breed. 22, 39
50. Bhatnagar, P., Minocha, R., Minocha, S., 2002. Genetic manipulation of the metabolism of polyamines in poplar cells: the regulation of putrescine catabolism. Plant Physiol. 128, 1455
1469. Bibi, A.C., Oosterhuis, D.M., Gonias, E.D., 2010. Exogenous application of putrescine ameliorates the effect of high temperature in Gossypium hirsutum L. flowers and fruit development. J. Agron. Crop Sci. 196, 205
211. Borrell, A., Bestford, T., Altabella, T., Masgrau, C., Tiburcio, A.F., 1996. Regulation of arginine decarboxylase by spermine in osmotically-stressed oat leaves. Physiol. Plant 98, 105
110. Bouchereau, A., Aziz, A., Larher, F., Martin-Tanguy, J., 1999. Polyamines and environmental challenges: recent development. Plant Sci. 140, 103
125. Camacho-Cristobal, J.J., Maldonado, J.M., Gonzalez-Fontes, A., 2005. Boron deficiency increases putrescine levels in tobacco plants. J. Plant Physiol. 162, 921
928. Capell, T., Bassie, L., Christou, P., 2004. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Nat. Acad. Sci. U.S.A. 101, 9909
9914. Chattopadhayay, M.K., Tiwari, B.S., Chattopadhyay, G., Bose, A., Sengupta, D.N., Ghosh, B., 2002. Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol. Plant. 116, 192
199. Cheng, L., Zou, Y., Ding, S., Zhang, J., Yu, X., Cao, J., et al., 2009. Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J. Integr. Plant Biol. 51, 489
499.

Plant Life under Changing Environment

References

493

Choudhary, S.P., Bhardwaj, R., Gupta, B.D., Dutt, P., Gupta, R.K., Kanwar, M., et al., 2010. Changes induced by Cu21 and Cr61 metal stress in polyamines, auxins, abscisic acid titers and antioxidative enzymes activities of radish seedlings. Braz. J. Plant Physiol. 22, 263
270. Christmann, A., Hoffmann, T., Teplova, I., Grill, E., Mu¨ller, A., 2005. Generation of active pools of abscisic acid revealed by in vivo imaging of water stresses Arabidopsis. Plant Physiol. 137, 209
219. Cona, A., Rea, G., Angelini, R., Federico, R., Tavladoraki, P., 2006. Functions of amine oxidases in plant development and defence. Trends Plant Sci. 11, 80
88. Cuevas, J.C., Lopez-Cobollo, R., Alcazar, R., Zarza, X., Koncz, C., Altabella, T., et al., 2008. Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating ABA levels in response to low temperature. Plant Physiol. 148, 1094
1105. Cvikrova´, M., Gemperlova´, L., Martincova´, O., Vankova´, R., 2013. Effect of drought and combined drought and heat stress on polyamine metabolism in proline-overproducing tobacco plants. Plant Physiol. Biochem. 73, 7
15. Duan, J.J., Li, J., Guo, S.R., Kang, Y.Y., 2008. Exogenous spermidine affects polyamine metabolism in salinitystressed Cucumis sativus roots and enhances short-term salinity tolerance. J. Plant Physiol. 165, 1620
1635. Eller, M.H., Warner, A.L., Knap, H.T., 2006. Genomic organization and expression analyses of putrescine pathway genes in soybean. Plant Physiol. Biochem. 44, 49
57. Flores, H.E., Galston, A.W., 1984. Osmotic stress-induced polyamine accumulation in cereal leaves: I. Physiological parameters of the response. Plant Physiol. 75, 102
109. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., et al., 2006. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9, 436
442. Galston, A.W., Sawhney, R.K., 1990. Polyamines in plant physiology. Plant Physiol. 94, 406
410. Garcıa-Jimenez, P., Just, P.M., Delgado, A.M., Robaina, R.R., 2007. Transglutaminase activity decrease during acclimation to hyposaline conditions in marine seaweed Grateloupia doryphora (Rhodophyta, Halymeniaceae). J. Plant Physiol. 164, 367
370. Garnica, M., Houdusse, F., Yvin, J.C., Garcia-Mina, J.M., 2009. Nitrate supply induces changes in polyamine content and ethylene production in wheat plants grown with ammonium. J. Plant Physiol. 166, 363
374. Gill, S.S., Tuteja, N., 2010. Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 51, 26
33. Groppa, M.D., Benavides, M.P., 2008. Polyamines and abiotic stress: recent advances. Amino Acids 34, 35
45. Groppa, M.D., Benavides, M.P., Tomaro, M.L., 2003. Polyamine metabolism in sunflower and wheat leaf discs under cadmium or copper stress. Plant Sci. 161, 481
488. He, L., Nada, K., Kasukabe, Y., Tchibana, S., 2002. Enhanced susceptibility of photosynthesis to low temperature photoinhibition due to interruption of chill-induced increase of S-adenosylmethionine decarboxylase activity in leaves of spinach (Spinacia oleracea L.). Plant Cell Physiol. 43, 196
206. Hu, W.W., Gong, H., Pua, E.C., 2005. The pivotal roles of the plant S-adenosylmethionine decarboxylase 50 untranslated leader sequence in regulation of gene expression at the transcriptional and posttranscriptional levels. Plant Physiol. 138, 276
286. Hummel, I., Gouesbet, G., El Amrani, A., Ainouche, A., Couee, I., 2004. Characterization of the two arginine decarboxylase (polyamine biosynthesis) paralogues of the endemic subantarctic cruciferous species Pringlea antiscorbutica and analysis of their differential expression during development and response to environmental stress. Gene 342, 199
209. Hussain, S.S., Ali, M., Ahmad, M., Siddique, K.H.M., 2011. Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol. Adv. 29, 300
311. Ioannidis, N.E., Kotzabasis, K., 2007. Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. Biochim. Biophys. Acta 1767, 1372
1382. Ioannidis, N.E., Sfichi, L., Kotzabasis, K., 2006. Putrescine stimulates chemiosmotic ATP synthesis. Biochim. Biophys. Acta—Bioenerg. 1757, 821
828. Iqbal, M., Ashraf, M., 2005. Changes in growth, photosynthetic capacity, and ionic relations in spring wheat (Triticum aestivum L.) due to pre-sowing seed treatment with polyamines. Plant Growth Regul. 46, 19
30. Jime´nez-Bremont, J.F., Ruiz, O.A., Rodrı´guez-Kessler, M., 2007. Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol. Biochem. 45, 812
821. Kasinathan, V., Wingler, A., 2004. Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Plant Physiol. 121, 101
107.

Plant Life under Changing Environment

494

18. Role of polyamines in plants abiotic stress tolerance: Advances and future prospects

Kasukabe, Y., He, L., Nada, K., Misawa, S., Ihara, I., Tachibana, S., 2004. Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stressregulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol. 45, 712
722. Kasukabe, Y., Lixiong, H., Yuriko, W., Motoyasu, O., Shimada, T., Tachibana, S., 2006. Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnol. 23, 75
83. Kaur-Sawhney, R., Tiburcio, A.F., Altabella, T., Galston, A., 2003. Polyamines in plants: an overview. J. Cell Mol. Biol. 2, 1
12. Knott, J.M., Ro¨mer, P., Sumper, M., 2007. Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett. 581, 3081
3086. Kuehn, G.D., Rodriguez-Garay, B., Bagga, S., Phillips, G.C., 1990. Novel occurrence of uncommon polyamines in higher plants. Plant Physiol. 94, 855
857. Kusano, T., Yamaguchi, K., Berberich, T., Takahashi, Y., 2007. Advances in polyamine research in 2007. J. Plant Res. 120, 345
350. ´ Z., et al., 2004. Cytological Kuthanova´, A., Gemperlova´, L., Zelenkova´, S., Eder, J., Macha´cˇ kova´, I., Opatrny, changes and alterations in polyamine contents induced by cadmium in tobacco BY-2 cells. Plant Physiol. Biochem. 42, 149
156. Kuznetsov, V.I., Shevyakova, N.I., 2007. Polyamines and stress tolerance of plants. Plant Stress 1, 50
71. Lee, T.M., 1997. Polyamine regulation of growth and chilling tolerance of rice (Oryza sativa) roots cultured in vitro. Plant Sci. 122, 111
117. Lefevre, I., Gratia, E., Lutts, S., 2001. Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci. 16, 943
952. Legocka, J., Kluk, A., 2005. Effect of salt and osmotic stress on changes in polyamine content and arginine decarboxylase activity in Lupinus luteus seedlings. J. Plant Physiol. 162, 662
668. Liu, K., Fu, H.H., Bei, Q.X., Luan, S., 2000. Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol. 124, 1315
1325. Liu, H.H., Dong, B.H., Zhang, Y.Y., Liu, Z.P., Liu, Y.L., 2004. Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings. Plant Sci. 166, 1261
1267. Liu, J.H., Nada, K., Honda, C., Kitashiba, H., Wen, X.P., Pang, X.M., et al., 2006. Polyamine biosynthesis of apple callus under salt stress: importance of arginine decarboxylase pathway in stress response. J. Exp. Bot. 57, 2589
2599. Liu, J.H., Kitashiba, H., Wang, J., Ban, Y., Moriguchi, T., 2007. Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol. 24, 117
126. Mahajan, S., Tuteja, N., 2005. Cold, salinity and drought stresses: an overview. Arch. Biophys. 444, 139
158. Martin-Tanguy, J., 2001. Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul. 34, 135
148. Moschou, P.N., Delis, I.D., Paschalidis, K.A., Roubelakis-Angelakis, K.A., 2008. Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiol. Plant. 133, 140
156. Murkowski, A., 2001. Heat stress and spermidine: effect on chlorophyll fluorescence in tomato plants. Biol. Plant. 44, 53
57. Najmeh, N., Ehsan, S., Ghorbanali, N., 2012. Salt-induced reduction in shoot spermine pool of Aeluropus littoralis. Adv. Environ. Biol. 6, 1765
1768. Navakouidis, E., Lu¨tz, C., Langebartels, C., Lu¨tz-Meindl, U., Kotzabasis, K., 2003. Ozone impact on the photosynthetic apparatus and the protective role of polyamines. Biochem. Biophys. Acta 1621, 160
169. Nayyar, H., 2005. Putrescine increases floral retention, pod set and seed yield in cold stressed chickpea. J. Agron. Crop Sci. 191, 340
345. Nayyar, H., Chander, S., 2004. Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J. Agron. Crop Sci. 190, 355
365. Ndayiragije, A., Lutts, S., 2006. Do exogenous polyamines have an impact on the response of a salt-sensitive rice cultivar to NaCl? J. Plant. Physiol. 163, 506
516. ¨ ztu¨rk, Z.N., Talame, V., Deyholos, M., Michalowski, C.B., Galbraith, D.W., Gomukirmizi, N., et al., 2002. O Monitoring large-scale changes in transcript abundance in drought- and salt-stresses barley. Plant Mol. Biol. 48, 551
573.

Plant Life under Changing Environment

References

495

Paschalidis, K.A., Roubelakis-Angelakis, K.A., 2005. Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant. Correlations with age, cell division/ expansion, and differentiation. Plant Physiol. 138, 142
152. Pathak, M.R., da Silva, J.A.T., Wani, S.H., 2014. Polyamines in response to abiotic stress tolerance through transgenic approaches. GM Crops Food 5 (2), 87
96. Pere´z-Amador, M.A., Leon, J., Green, P.J., Carbonell, J., 2002. Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol. 130, 1454
1463. Racz, I., Paldi, E., Szalai, G., Janda, T., Pal, M., Lasztity, D., 2008. S-Methylmethionine reduces cell membrane damage in higher plants exposed to low-temperature stress. J. Plant Physiol. 165, 1483
1490. Rengasamy, P., 2006. World salinization with emphasis on Australia. J. Exp. Bot. 57, 1017
1023. Richards, F.J., Coleman, R.G., 1952. Occurrence of putrescine in potassium-deficient barley. Nature 170, 460. Rider, J.E., Hacker, A., Mackintosh, C.A., Pegg, A.E., Woster, P.M., Casero Jr., R.A., 2007. Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33, 231
240. Rodrıguez-Kessler, M., Ruiz, O.A., Maiale, S., Ruiz- Herrera, J., Jimenez-Bremont, J.F., 2008. Polyamine metabolism in maize tumors induced by Ustilago maydis. Plant Physiol. Biochem. 46, 805
814. Roy, M., Ghosh, B., 1996. Polyamines, both common and uncommon, under heat stress in rice (Oryza sativa) callus. Physiol. Plant. 98, 196
200. Sagor, G.H., Berberich, T., Takahashi, Y., Niitsu, M., Kusano, T., 2013. The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Res. 22, 595
605. Sasaki, Y., Asamizu, E., Shibata, D., Nakamura, Y., Kaneko, T., Awai, K., et al., 2001. Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res. 8, 153
161. Sebela, M., Radova, A., Angelini, R., Tavladoraki, P., Frebort, I., Pec, P., 2001. FAD-containing polyamine oxidases: a timely challenge for researchers in biochemistry and physiology of plants. Plant Sci. 160, 197
207. Sfakianaki, M., Sfichi, L., Kotzabasis, K., 2006. The involvement of LHCII-associated polyamines in the response of the photosynthetic apparatus to low temperature. J. Photochem. Photobiol. B: Biol. 84, 181
188. Shi, H., Chan, Z., 2014. Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J. Integr. Plant Biol. 56, 114
121. Shu, S., Guo, S.R., Sun, J., Yuan, L.Y., 2012. Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiol. Plant. 146, 285
296. Simon-Sarkadi, L., Kocsy, G., Va´rhegyi, A., Galiba, G., de Ronde, J.A., 2006. Effect of drought stress at supraoptimal temperature on polyamine concentrations in transgenic soybean with increased proline levels. Z. Naturforsch. C 61, 833
839. Slocum, R.D., 1991. Polyamine biosynthesis in plants. In: Slocum, R.D., Flores, H.E. (Eds.), Biochemistry and Physiology of Polyamines in Plants. CRC Press, Boca Raton, FL, pp. 22
40. Sood, S., Nagar, P.K., 2005. Alterations in endogenous polyamines in bulbs of tuberose (Polianthes tuberose L.) during dormancy. Sci. Hortic. 105, 483
490. Szalai, G., Pap, M., Janda, T., 2009. Light-induced frost tolerance differs in winter and spring wheat plants. J. Plant Physiol. Available from: https://doi.org/10.1016/j.jplph.2009.04.016. Tang, W., Newton, R.J., 2005. Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant. Growth Regul. 46, 31
43. Tiburcio, A.F., Wollenweber, B., Zilberstein, A., Koncz, C., 2012. Abiotic stress tolerance. Plant Sci. 182, 1
2. Tuteja, N., 2009. Cold, salinity, and drought stress. In: Hirt, H. (Ed.), Plant stress biology, from genomics towards system biology. Wiley-Blackwell Inc, Weinheim, Germany, pp. 137
159. Urano, K., Yoshiba, Y., Nanjo, T., Igarashi, Y., Seki, M., Sekiguchi, F., et al., 2003. Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ. 26, 1917
1926. Valero, D., Perez-Vicente, A., Martinez-Romero, D., Castillo, S., Guillen, F., Serrano, M., 2002. Plum storability improved after calcium and heat postharvest treatments: role of polyamines. J. Food Sci. 67, 2571
2575. Vergnolle, C., Vaultier, M.N., Taconnat, L., Renou, J.P., Kader, J.C., Zachowski, A., et al., 2005. The cold-induced early activation of phospholipase C and D pathways determines the response of two distinct clusters of genes in Arabidopsis cell suspensions. Plant Physiol. 139, 1217
1233.

Plant Life under Changing Environment

496

18. Role of polyamines in plants abiotic stress tolerance: Advances and future prospects

Verma, S., Mishra, S.N., 2005. Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J. Plant Physiol. 162, 669
677. Wang, X., Shi, G., Xu, Q., Hu, J., 2007. Exogenous polyamines enhance copper tolerance of Nymphoides peltatum. J. Plant Physiol. 164, 1062
1070. Wang, J., Sun, P.P., Chen, C.L., Wang, Y., Fu, X.Z., Liu, J.H., 2011. An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J. Exp. Bot. 62, 2899
2914. Watson, M.B., Malmberg, R.L., 1996. Regulation of Arabidopsis thaliana (L.) Heynh Arginine decarboxylase by potassium deficiency stress. Plant Physiol. 111, 1077
1083. Watson, M.B., Emory, K.K., Piatak, R.M., Malmberg, R.L., 1998. Arginine decarboxylase (polyamine synthesis) mutants of Arabidopsis thaliana exhibit altered root growth. Plant J. 13, 231
239. Wei, G.P., Yang, L.F., Zhu, Y.L., Chen, G., 2009. Changes in oxidative damage, antioxidant enzyme activities and polyamine contents in leaves of grafted and nongrafted eggplant seedlings under stress by excess of calcium nitrate. Sci. Hortic. 120, 443
451. Weinstein, L.H., Kaur-Sawhney, R., Rajam, M.V., Wetilaufer, S.H., Galston, A.W., 1986. Cadmium-induced accumulation of putrescine in oat and bean leaves. Plant Physiol. 82, 641
645. Wen, X.P., Pang, X.M., Matsuda, N., Kita, M., Inoue, H., Hao, Y.J., et al., 2008. Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res. 17, 251
263. Wen, X.P., Ban, Y., Inoue, H., Matsuda, N., Moriguchi, T., 2010. Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic European pear by exerting antioxidant activities. Transgenic Res. 19, 91
103. Wi, S.J., Park, K.Y., 2002. Antisense expression of carnation cDNA encoding ACC synthase or ACC oxidase enhances polyamine content and abiotic stress tolerance in transgenic tobacco plants. Mol. Cells 13, 209
220. Wi, S.J., Kim, W.T., Park, K.Y., 2006. Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants. Plant Cell Rep. 25, 1111
1121. Xiong, H., Stanly, B.A., Tekwani, B.L., Pegg, A.E., 1997. Processing of mammalian and plant S-adenosylmethionine decarboxylase proenzymes. J. Biol. Chem. 272, 28342
28348. Yamaguchi, K., Takahashi, Y., Berberich, T., Imai, A., Miyazaki, A., Takahashi, T., et al., 2006. The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett. 580, 6783
6788. Yamaguchi, K., Takahashi, Y., Berberich, T., Imai, A., Takahashi, T., Michael, A.J., et al., 2007. A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem. Biophys. Res. Commun. 352, 486
490. Yang, J., Zhang, J., Liu, K., Wang, Z., Liu, L., 2007. Involvement of polyamines in the drought resistance of rice. J. Exp. Bot. 58, 1545
1555. Yang, H.Y., Shi, G.X., Qiao, X.Q., Tian, X.L., 2011. Exogenous spermidine and spermine enhance cadmium tolerance of Potamogeton malaianus. Russ. J. Plant Physiol. 58, 622
628. Yiu, J.C., Juang, L.D., Fang, D.Y.T., Liu, C.W., Wu, S.J., 2009. Exogenous putrescine reduces flooding-induced oxidative damage by increasing the antioxidant properties of Welsh onion. Sci. Hortic. 120, 306
314. Zapata, P.J., Serrano, M., Pretel, M.T., Amoros, A., Botella, M.A., 2004. Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci. 167, 781
788. Zeid, I.M., Shedeed, Z.A., 2006. Response of alfalfa to putrescine treatment under drought stress. Biol. Plant. 50, 635
640. Zhang, W., Jiang, B., Li, W., Song, H., Yu, Y., Chen, J., 2009. Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Sci. Hortic. 122, 200
208. Zhao, F., Song, C.P., He, J., Zhu, H., 2007. Polyamines improve K1/Na1 homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol. 145, 1061
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19 The role of sugars in the regulation of environmental stress Nimisha Amist and N.B. Singh Plant Physiology Laboratory, Department of Botany, University of Allahabad, Prayagraj, India

19.1 Introduction The main reason behind the existence of life on the Earth is the production of oxygen along with energy-rich sugar molecules due to fixation of carbon and light energy through photosynthesis. Plants are autotrophs with the ability to produce sugars through photosynthesis and also utilize the produced carbohydrates. Sugars are universally distributed in plants and are the rich source of carbon and energy in eukaryotes. Soluble sugars, namely, sucrose, glucose and fructose, play an important role in preserving the structure and growth of plants (Rosa et al., 2009). The regulation of sugars in plants is a complex process as it occurs at specific sites and definitely requires long-distance signaling in order to synchronize with altered physiological, developmental, and environmental conditions (Lemoine et al., 2013). Sugar molecules along with being a nutrient also function as main regulator for major functions, such as metabolism, growth, stress responses, and participate in general development of plant body from the stage of embryogenesis to senescence (O’Hara et al., 2013). Sugars also actively participate in photosynthesis, carbon partitioning, osmotic homeostasis, protein synthesis, membranes stabilization (Hoekstra et al., 2001), and gene expression in response to abiotic stresses (Rosa et al., 2009). Environmental factors influence the distribution of plants. Among environmental factors, drought, salinity, and extreme temperatures are the most important that have evolved with plants; however, other factors, such as heavy metals, ultraviolet-B radiation, flooding, and atmospheric pollutants, acquired a pertinent attention (Grata˜o et al., 2005; Mittler, 2006). Plants have evolved an array of adaptive strategies to evade environmental stresses for survival. Responses to a definite stress vary within the plant, but some common reactions happen in all plants. Soluble sugars are extremely responsive to environmental stresses, which proceed on affecting the delivery of carbohydrates from source to sink organs. Both sucrose and hexoses are engaged in dual activities of regulation of gene as evinced

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by the upregulation and downregulation of both growth-related and stress-related genes, respectively. Increased concentration of soluble sugars enhances plant tolerance to numerous abiotic stresses, such as drought, salinity, and cold (Rathinasabapathi, 2000). Therefore the study of wide range of sugar level under abiotic stresses is a promising field of research that needs to be explored as it often plays a crucial role in conferring tolerance against abiotic stresses by modulating several physiological processes (Rathinasabapathi, 2000). This chapter focuses on evaluating physiological and molecular mechanisms that are synchronized by sugars in concentration-dependent manner. In addition to this, special focus has been invested in discussing connection between sugars, oxidative stress, antioxidant system, and ameliorative role of sugars in plants under abiotic stress.

19.1.1 Plant growth and development Glucose and fructose actively participate in cell division, while differentiation and maturation are regulated by sucrose (Koch, 2004). The processes, such as cell division, cell expansion, and increase in reserve carbohydrate, are regulated by glucose and sucrose in developing plant embryos (Borisjuk et al., 2003; Yaseen et al., 2013). Increased concentration of soluble sugars triggered the propagation of organs and produced larger and thicker leaves (Gibson, 2005). High sugar accumulation caused increase in the size and number of tubers in potatoes, enhanced adventitious roots formation in Arabidopsis, and also promoted cell division and cell expansion and storage during embryogenesis in legumes. However, it was observed that elevated level of glucose and sucrose repressed cotyledon expansion, formation of true leaf and root growth in young Arabidopsis seedlings (Gibson, 2005). Glucose and sucrose have been found to actively participate in different parts of the life cycle of plant. Eveland and Jackson (2011) reported that glucose was extremely active in nondifferentiated cells and participates in cell division, whereas sucrose stimulated cell division and synthesis of starch in mature cells (Borisjuk et al., 2003). Seedling growth rate was stimulated under the exogenous application of glucose in culture medium (Harvais and Hardley, 1967).

19.1.2 Role of sugars in processes of plants physiology 19.1.2.1 Photosynthesis Photosynthesis is an essential process linked with the manufacture of sugars so as to control growth and development of plants (Smeekens, 2000). Accumulation of high sugar levels causes inhibition in photosynthesis (Jang et al., 1997) leading to stunted growth and necrosis in leaves (Sonnewald et al., 1991). Low sugar levels elevate rate of photosynthesis, mobilize reserves materials, whereas high sugar concentrations endorse carbohydrate storage and growth (Rolland et al., 2002) (Table 19.1). 19.1.2.2 Senescence Doorn (2008) reported that soluble sugars affect a variety of functions including the commencement of senescence. High carbon and low nitrogen have been found to

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TABLE 19.1 Impact of exogenous glucose application on physiological processes of plants. Exogenous glucose treatment Effects under high concentration

Effects under low concentration

1. 2. 3. 4.

1. 2. 3. 4.

Delayed seed germination Inhibition of photosynthesis Delay in flowering Acceleration in senescence

Promotes seed germination Stimulation of photosynthesis Stimulates flowering Delay in senescence

accelerate senescence. The combined treatment of glucose and nitrogen in low amount induced leaf senescence in Arabidopsis plants (Wingler et al., 2006), and glucose and low nitrogen promoted the accumulation of glucose more strongly in light compared to dark (Paul and Driscoll, 1997). Wingler et al. (2012) reported enhanced sugar accumulation in tobacco and Arabidopsis as the senescence proceeds in leaves. High level of CO2 accelerates senescence causing greater accumulation of sugars along with decline in the nitrogen and Rubisco content (Xu et al., 2015). 19.1.2.3 Seed germination Low concentration of glucose applied exogenously alleviates the harmful effects of glucose on seed germination, which are stimulated by abscisic acid (ABA) (Finkelstein and Lynch, 2000) (Table 19.1). Price et al. (2003) observed that elevated level of glucose delayed seed germination. Although low concentration of glucose did not inhibit seed germination but caused considerable delay in seed germination (Zhu et al., 2009). Gibson (2005) reported that high glucose concentration is very lethal to seedling growth and development. It has been postulated that high level of glucose induces ABA accumulation resulting into delay in seed germination (Arenas-Heurtero et al., 2000; Gill et al., 2003). However, later studies proved that elevated intensity of glucose in fact decreases the rate of disintegration of endogenous ABA of rather than causing accretion of ABA (Price et al., 2003). Soluble sugars, such as galactose, maltose, and trehalose, may not be efficient in delaying germination, but glucose alone or in combination with other sugars has an inherent capability of postponing seed germination or premature seedling development (Dekkers et al., 2004; Gibson, 2005). 19.1.2.4 Flowering Flowering in plants is significant developmental phase that is affected by sugars. A significant delay in flowering in response to high level of glucose was reported, but low glucose concentration stimulates flowering (Smeekens et al., 2010) (Table 19.1). Flowering in plants depends upon photoperiodic dark period. Exogenous application of sugars seems to affect flowering time in many plant species (Bernier et al., 1993). Various studies have reported that elevated sucrose participates in the induction of flowering. The optimum level of sucrose and nitrogen promoted flowering in tomato (Dielen et al., 2001). Ohto et al. (2001) reported concentration-dependent stimulatory and inhibitory effects of sucrose on flowering and floral transitions.

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19.1.2.5 Hypocotyl growth Exogenously applied sucrose had inhibited the growth of hypocotyls but stimulated the root growth of Brassica napus. The elongation of hypocotyl in the dark and opening of cotyledons in light are obstructed due to high concentration of sugars (Jang et al., 1997). Sugars are often linked with a twofold event happening in plants. It was observed that glucose and sucrose inhibited hypocotyl elongation Arabidopsis seedlings that grown in dark (Price et al., 2004; Gibson, 2005).

19.1.3 Sugar sensing and signaling Sensor proteins are responsible for detecting the status of sugar in plant cells. A sugar molecule and a sensor protein interact within themselves to generate a signal. The signaltransduction cascades are initiated due to signal molecule resulting into cellular responses such as changed gene expression and enzymatic activities. All stages pertaining to the development of plants beginning from seed germination to seed development are affected. Sugars act as signal molecule, similar to hormones, operate as primary messengers, and also regulate signals that supervise the expression of different genes concerned with sugar metabolism. Sugar sensing has been suggested to occur through hexose. Two pathways of hexose sensing have been postulated: hexokinase (HXK) dependent and the other HXK independent. Plants have both HXK-dependent and -independent sugar signaling pathways. The phosphorylation of sugars is an important necessity of HXK-dependent system, while the independent system only requires sugars (Smeekens, 2000). Sugars function as regulatory signals that direct the expression of variety of genes concerned with many processes (Lalonde et al., 1999; Roitsch, 1999). The suppression of photosynthetic genes by the HXKphosphorylated sugar analogs provided substantiation in favor of HXK-dependent signaling (Jang and Sheen, 1994). Furthermore, 2-deoxy glucose (2-DG) and 2-deoxy mannose have been known to cause repression even though they cannot be synthesized after phosphorylation. The downstream glucose metabolic pathways and sugar signaling pathways don’t hinder each other. The prospect of glucose being transformed to other derivatives thus activating suppression of photosynthetic genes without undergoing phosphorylation has been ruled out (Jang and Sheen, 1994). Glucose-6-phosphate (G-6-P) has been revealed to operate as repressive signal molecule (Brun et al., 1993). In fact, direct release of sugar phosphates to cells did not cause oppression of photosynthetic genes (Jang and Sheen, 1997). Glucose treatment did not cause elevation in the intracellular level of G-6-P signifying that glucose behaves as direct signal. Mannoheptulose, an aggressive inhibitor of HXK blocked the rigorous suppression caused by 2-DG. All the previous observations indicated that HXK functions as a sensor in mediating the repression signal. The genes encoding cell-wall invertase, sucrose synthase, and phenylalanine ammonia-lyase are activated through glucose analog 6-DG. 6-DG can be easily transported across plasma membrane but is not phosphorylated by HXK thus providing evidence for HXK-independent signaling pathways (Roitsch et al., 1995; Godt and Roitsch, 1997). Xiao et al. (2000) suggested three signal-transduction pathways for glucose in plants. These are AtHXK1-dependent pathway present in Arabidopsis thaliana in which

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AtHXK1-mediated signaling function was correlated with the gene expression. The second one is glycolysis-dependent pathway that is subjective to catalytic activities of both AtHXK1 and heterologous yeast HXK2. The third pathway is HXK-independent pathway which is free of AtHXK1 for gene expression. The modification in conformation due to substrate binding consequently initiates signaling cascade, and this mechanism has been proposed for glucose sensing via HXK1 (Harrington and Bush, 2003). Although exact mechanism whether HXK senses glucose in concentration-dependent manner or as flux sensor is not clear. Hexose sensing and signaling functions depend upon subcellular localization, translocation, and interactions with downstream effectors of HXK (Rolland et al., 2002). The repression at m-RNA level and inhibition in proton sucrose symporter transport activity has been attributed to the signaling function of sucrose (Barker et al., 2000). It is very difficult to assay the mechanism involved sugar signal-transduction pathways due to dual role of sugars as a nutrient and a signaling (Rolland et al., 2001).

19.1.4 Signal-transduction cascades Very little information is available about the impact that sugars have on the expression of genes concerned in sugar signaling cascade. The sugar sensors present signaling information to signal-transduction cascades that generate a range of plant responses. The signal-transduction cascades involved in sugar regulated signaling are mitogen-activated protein kinases, protein phosphatases, Ca21, and calmodulin (Barker et al., 2000). Glucose modulated expression of a number of genes concerned in ABA biosynthesis and also in the post germination response of glucose (Cheng et al., 2002). Sugar stimulated the induction of genes in sweet potato as well as expression of reporter gene, that is, β-amylase promotor-iudA (Amy-Gus) fusion genes in tobacco has been blocked by the specific inhibitors of protein-Ser/Thr phosphatases. Staurosporine, an inhibitor of Ser/Thr protein kinase, inhibited Amy-Gus gene expression in response to sugar in tobacco (Ohto and Nakamura, 1995). Sugar-induced calcium-dependent (calmodulin domain) Ser/Thr protein kinase (CDPK) has also been reported to be connected with the plasma membrane of leaf tissues in tobacco (Ohto and Nakamura, 1995). Sugars suppressed the expression of RUBISCO, a source-specific gene, but the induction of CIN (sink specific) and PAL (pathogen induced) genes occurred in Chenopodium rubrum (Ehness et al., 1997). These genes were found to be synchronized by glucose in an HXKindependent pathway. In fact, glucose-mediated regulation of these genes was imitated by different protein phosphatase inhibitors (Smeekens, 2000). Thus it reflected the role of protein dephosphorylation in transduction of the sugar signal. The expression of the genes, which encode sucrose metabolizing enzymes and also hexose and sucrose transporters, has helped in establishing evidence for involvement of sugars in various stages of seed development (Tegeder et al., 1999; Loreti et al., 2001). HXK is able to establish the flux of hexoses entering glycolysis, while sucrose transporters operate as sensors for disaccharide and also help in sensing the level of apoplastic sugar along with regulating the flux of sugars passing through plasma membrane (Lalonde et al., 1999).

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Role of sugar sensing has been recognized during germination in rice. Increased glucose level caused downregulation of α-amylase gene expression through a process that involves sugar sensing. HXK has been found to be involved in transmitting the glucose signal. Glucosamine, an inhibitor of HXK, repressed the HXK substrate 2-DG-induced signaling. α-amylase expression was repressed during barley seed germination by hexoses that were specifically substrates for HXK (Perata et al., 1997). The expression of α-amylase genes in the presence of gibberellic acid (GA) is regulated by sugars. Sugars have been associated with the repression of genes involved in the stimulation of α-amylase in germinating barley seeds and cotyledons of deembryonated cowpea (Morita et al., 1998; Kaur et al., 2005). The elements responsive to sugar and GA in the promoter of the Ramy gene seems to overlap, indicating that the two signal-transduction pathways correspond at a point upstream of the promoter elements (Morita et al., 1998). Glucose is an effective modulator in activating the genes implicated in ABA biosynthesis during germination (Price et al., 2003) and also represses the genes related with ABA catabolism (Zhu et al., 2009). Elevated level of sugars triggers the suppression of genes related to photosynthesis (Hammond et al., 2011), as a result sugar accumulation leads to the decline of photosynthesis (Pego et al., 2000). The export of sugars was inhibited in response to several environmental factors, therefore sugar accumulation occurs in leaf leading to suppression of genes related with photosynthesis (Krapp et al., 1993). High sugar concentration downregulated the expression of chlorophyll a/b binding protein gene in Chenopodium, maize and pea (Krapp et al., 1993; Knight and Gray, 1995). Sugars also downregulated genes that controlled the expression of C4 cycle enzymes such as C4 malic enzyme gene (ME1), C4 PEP carboxylase (PEPC1) gene, and pyruvate phosphate dikinase gene in maize (Sheen, 1990). An elevation of up to 100-fold has been recorded in the expression of senescence-associated genes in response to exogenous application of glucose and low nitrogen (Wingler et al., 2006). HXK-dependent signaling is involved in accelerated leaf senescence by glucose and low nitrogen (Wingler et al., 2006).

19.1.5 Sugars and abiotic stress interaction in plants Among the many environmental factors that can affect plant growth, this chapter concentrates on the following effects (Fig. 19.1). 19.1.5.1 Effects of water deficit Water deficit is a chief abiotic factor disturbing crop development and yield. Drought imposes hostile circumstances on the leaves (source organs) and roots (sink organs) of a plant. Turgeon (2010) stated that maintenance of elevated osmotic potential in the phloem cells acts as positive factor toward attracting water to the sieve tubes and consequently sustains phloem sap current in drought conditions. The whole structural design of plants is modified under drought stress. Mild water deficit restricts shoot growth but root growth continues. In dicots the quantity of branches and leaves on branches are predominantly susceptible to soil water deficit (Lecoeur et al., 1995; Lebon et al., 2006), while a number of young emerging organs in monocots are reduced under drought (Courtois et al., 2000).

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FIGURE 19.1 Sugars and abiotic stress interaction in plants.

Often water-stress escaping strategy causes decrease in photosynthetic productivity thus affecting the carbon flow to different sink organs. Drought is known to hampers photosynthesis significantly (Ashraf and Harris, 2013). Most researches on the effect of water deficit on sugar metabolism showed that carbohydrate levels were altered in the plant leaves. Starch levels decrease, while sucrose and hexose amounts increase (Pelleschi et al., 1997) reflecting that initiation of starch hydrolysis and sucrose synthesis occurs in response to drought stress. It has been hypothesized that accumulated sucrose in the leaves in response to water stress provides energy supply for preservation of cell during high respiration rate in environments (Burke, 2007). Soluble sugar helps in maintaining the leaf water content and osmotic adjustment of plants subjected to drought stress (Xu et al., 2007). However, decreased utilization of sugar due to restriction of growth may also cause accumulation of sugars in leaves (Hummel et al., 2010). Water deficit induces alterations in the intensity of the main organic nutrients, that is, sugars and amino acids inside the sieve tubes. Analysis of phloem sap of alfalfa indicated a considerable augmentation in sucrose and total amino-acid contents resulting into decline of leaf water potential from 20.4 to 22.0 MPa. Larger amounts of Val, Leu, Ile, Glu, Asp, Thr, and particularly Pro have altered the concentration of total amino acid (Girousse et al., 1996). Water stress resulted in increase of sucrose and Pro levels in phloem sap collected from Arabidopsis leaves (Mewis et al., 2012). The negative impact of drought on sink organs have been reported in potato tubers, as sucrose biosynthesis was promoted under osmotic stress instead of starch biosynthesis via the stimulation of sucrose-phosphate synthase and the inhibition of ADP-glucose pyrophosphorylase (Geigenberger et al., 1997). The decline in stored carbohydrates such as starch and fructans in stems has been linked to enhanced starch content of grains

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(Yang et al., 2004). It has been reported that drought caused decrease in cytosolic invertase activity in the seeds, but the activity of invertases present in vacuole and cytosol increased in leaves, signifying that the available amounts of sucrose for transfer to the seeds are reduced under drought (Trouverie et al., 2004). The harmful impact of dryness on the ratio of sink/source is injurious to crop production in terms of biomass relocation (CuellarOrtiz et al., 2008). Drought stress induces senescence and enhances mobilization of reserve materials (Chandlee, 2001). The strategies adopted by plant in order to mitigate stress involve senescence and reserve mobilization both being essential mechanism of plant development (Cowan et al., 2005). Overexpression of Arabidopsis HXK in tomato seedlings caused increase in sugar contents due to high level of HXK, eventually reducing the photosynthetic activity and increasing senescence in leaves (Dai et al., 1999). Allocation of assimilates in rice to developing grains was promoted, resulting into shortened grain filling and increased rate of grain filling due to drought-induced leaf senescence (Yang et al., 2002). In soybean, water reduction decrease seed size principally because of a restriction in the filling period rather than a reserve of the seed growth rate (Westgate et al., 1989). Grape yield decreased under drought, while total sugar content in the existing berries increased (Huglin, 1986). Sugars are involved in membrane protection and scavenging of radical during stress (Krasensky and Jonak, 2012). Sugar accumulation protects the cell membrane from oxidation in response to water deficiency (Arabzadeh, 2012). Sugar accumulation reduced the rate of photosynthesis under drought condition (Liu et al., 2004). Sugars protect the cells during drought by two mechanisms. In first mechanism the hydroxyl groups of sugars probably substitute for water and helps in maintaining hydrophilic interactions in membranes and proteins throughout dehydration period thus preventing protein denaturation; and in second mechanism, sugars contribute to vitrification, that is, biological glass is formed in the cytoplasm of dehydrated cells (Leopold, 1994). Soluble sugars help in maintaining the turgidity of leaves and avoid dehydration of membranes and proteins (Sawhney and Singh, 2002). Understanding of drought sensitivity at the critical stage of development is necessary for improving productivity of crop. 19.1.5.2 Effects of salinity (NaCl) Salt stress is considered as a major factor restricting plant growth and productivity due to poor water quality in many places of irrigation. Salt stress shares many character with drought stress as in both cases, the most important consequence is lower soil water potential around the roots. The initiation of stress in response to sodium toxicity is due to transport of salt inside the plant through the transpiration stream. Potassium channels help in circulation of Na1 inside the plant (Berthomieu et al., 2003). Na1 ion is loaded into the leaf phloem and transported to roots to be released as excretion, thus declining the level of Na1 in leaves (Berthomieu et al., 2003) although that flux may be insignificant in comparison to the xylem flux (Davenport et al., 2007). Little information is available about the effects of salt stress on transport of sucrose through the phloem. Salt stress negatively affects the photosynthesis (Suwa et al., 2008) and causes growth impairment, which is more evident in leaves than in roots (Lohaus et al., 2000). The concentration of sucrose in phloem was not affected by salt stress, but the level of amino acid and Na1 elevated in the sieve tubes. The increased root/shoot ratio under salt stress might be due to increased amount of amino acids delivered to the roots (Lohaus et al., 2000). However, in tomato,

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salt stress directly inhibits the sucrose loading and translocation in phloem, causing deficiency in partitioning of sucrose to the roots (Suwa et al., 2008). Salt stress altered the physiological processes of plants by decreasing photosynthesis, nitrogen assimilation, and cell division, thus ultimately arresting the plant growth (Anjum et al., 2011). High concentration of salt applied exogenously leads to the decrease in leaf growth, reduces conductance of stomata, causes disproportion of ion ratio, and inhibits photosynthesis (Wani et al., 2013). Accumulated sugar during salt stress serves as an osmolyte for mitigating the harmful effects (Almodares et al., 2008). It seems that increased level of sugars, such as glucose, sucrose, and fructose, in response to salinity helps in carbon storage and osmoprotection along with maintaining osmotic homeostasis and scavenging of free radicals (Rosa et al., 2009). In wheat seedlings, treatment with lower amount of glucose stimulates seed germination under saline conditions (Hu et al., 2012). Weak development of coleoptiles and radical are main reason of decline in seed germination under salinity (Prado et al., 2000). However, treatment with low level of glucose increases the growth of coleoptiles and radical and leads successful seed germination (Hu et al., 2012). Exogenous application of glucose under salt stress delimits annihilation of chlorophyll, enhances dry weight, maintains ionic homeostasis and accumulation of proline, prevents water loss, and activates activity of antioxidant enzyme (Hu et al., 2012). Pattanagul and Thitisaksakul (2008) reported glucose and fructose function as osmoprotectant and free radical scavenger in rice under salinity. Furthermore, oxidative pentose phosphate pathway seems to be participating in scavenging of reactive oxygen species (ROS) indicating that soluble sugars are associated with ROS anabolism and catabolism (Cuoee et al., 2006). Exogenously applied glucose inhibits Na1 accumulation but simultaneously enhances the uptake of K1 in wheat seedlings under salt stress thus consequently helps in maintaining ionic homeostasis during saline condition (Nemati et al., 2011). 19.1.5.3 Effects of light Light directly regulates phloem loading through photosynthesis by stimulating the synthesis of sucrose and providing energy. The anatomy of the loading zone is affected by light intensity (Amiard et al., 2005, 2007). Different approach toward light intensity was observed in plants on the basis of phloem-loading mechanism, that is, apoplastic or symplastic. Thus plants acclimatized to the increased photosynthesis differently. The cell-wall invaginations increased in the companion cells around sieve element in the species with apoplastic loading mechanism (Amiard et al., 2005). This modification indicates that enlarged exchange surface approved elevated sucrose phloem loading. However, in plant species with symplastic mechanism of phloem loading did not undergo modifications in plasmodesmatal frequencies, consequently causing starch accumulation in leaves (Amiard et al., 2005). Amiard et al. (2007) further investigated the mechanism behind the ability of apoplastic loaders to increase surface area in the conducting cell for enhanced membrane sucrose transfer. It has been hypothesized that cell-wall enlargement may also play role in protection of phloem cells against pathogenic attacks. 19.1.5.4 Effects of low temperatures Cold stress causes a considerable disturbance to the membranes, enhances ROS accumulation, protein denaturation, etc. (Mahajan and Tuteja, 2005; Yuanyuan et al., 2009).

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In higher plants, soluble sugars, such as glucose, sucrose, fructose, raffinose, and stachyose, are recognized to provide protection against freezing (Yuanyuan et al., 2009). The sugars function as defending agent against drought or chilling stress by protecting membranes through interactions with lipids in plasma membrane (Garg et al., 2002). Sugars operate as osmoprotectants. Fructans with high water solubility prevent the crystallization of cytoplasm under chilling (Livingston et al., 2009). Furthermore, fructans are in some way linked with osmotic adjustment along with stabilization of membranes in response to freezing and dehydration (Krasensky and Jonak, 2012). Usually, trehalose is reported in small quantities, but its concentration elevated drastically on exposure to stress (Fernandez et al., 2010). Trehalose functions as an osmolyte stabilizing protein’s structure and membranes (Eastmond and Graham, 2003). Cold stress elevated concentration of trehalose in rice (Garg et al., 2002). Freezing tolerance was enhanced in A. thaliana after exogenous application of sucrose (Li et al., 2006). Soluble sugars generally guard phospholipids present in membrane by inducing glass formation in the cytoplasm (Anchordoguy et al., 1987; Crowe et al., 1988). Low temperatures affect sugar transport through phloem in diverse ways and usually involve distinct cells such as intermediary cells, parenchyma transfer cells, and sieve elements. Symplastic loaders are affected more susceptible to cold in comparison to apoplastic loaders (Van Bel and Gamalei, 1992). In herbaceous species and deciduous trees, intermediary cells collapse under low temperatures, resulting into decreased carbohydrate loading thus directly elucidating the sensitivity of symplastic phloem loading under cold stress (Gamalei et al., 1994). However, these changes in structure were not observed in evergreen species with a symplastic phloem-loading mode. Consequently, the transport of excessive photoassimilates from source leaves might be compulsory for the sustainment of their functional and structural integrity, thus it can be regarded as cold adaptation (Hoffmann-Thoma et al., 2001). However, Schrier et al. (2000) revealed that there is no variation between species exhibiting symplastic and apoplastic mechanism of phloem loading in their reaction to cold. Thus it was hypothesized that the phloem loading was an approach that depends on habitat rather than on growth (Davidson et al., 2011). Tocopherol deficit impairs photoassimilate export from source leaves through elevated callose deposition in the vascular tissues in monocot and dicot plant species (Hofius et al., 2004). The similar consequence has also been described for phloem loading due to decrease in temperature (Maeda et al., 2006). 19.1.5.5 Oxidative stress and antioxidant system ROS generation and accretion has been directly linked with sugar accumulation for adaptation against ill effects of environmental stress (Roitsch, 1999). In addition, oxidative pentose phosphate pathway, which is involved in NADPH formation, is also responsible for scavenging of ROS indicating that soluble sugars are associated with ROS anabolism and catabolism (Hu et al., 2012). Increased ROS production caused elevation in membrane damage by producing substances such as malondialdehyde and thiobarbituric acid-reactive substances, which are implicated in lipid peroxidation, thus ultimately resulting in cell death (Ayala et al., 2014). Exogenous application of glucose in low concentration prevented lipid peroxidation under NaCl treatment (Hu et al., 2012). It seems that glucose possesses ability to scavenge excessive ROS produced as a result of

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abiotic stress even in low concentration; therefore it eliminates all the detrimental processes, such as disintegration of chlorophyll, membrane injury, and cell death. Sugars apart from glucose, such as sucrose, fructose, and trehalose play important role as osmoprotectants during the osmotic adjustment, give protection to membrane, and scavenge toxic ROS against different stresses (Singh et al., 2015). The activities of antioxidant enzymes have been stimulated in the presence of low concentration of soluble sugars, such as glucose and sucrose in response to stresses (Boriboonkaset et al., 2012; Hu et al., 2012).

19.1.6 Conclusions and future perspectives Physiological processes, such as normal plant growth, metabolism, development, and cell functions, are obstructed by abiotic stresses. Sugars have been accepted as a fresh group of metabolites well-known for numerous functions in plants. Evidently, the chief sugars such as glucose and sucrose are connected with numerous processes involved in metabolism, such as energy production, biosynthesis of polymers, production of metabolites, and regulation of source-sink activities. In this chapter, we have focused on the activity of accumulated sugars in generating stress tolerance in plants. Generally, sugars with their osmoprotectant activities help in stabilizing membranes under abiotic stress conditions. An enormous quantity of information is accessible on the participation of soluble sugars in various physiological processes under abiotic stress. Additional researches should concentrate on the impact of sugars on the enzymes activities and genes linked to physiological processes in plants. There is a need of extensive study to investigate the role of enzymes that either stimulated or inhibited due to sugar accumulation under stressful environment. Glucose and sucrose are the most vital sugars chiefly related with the process of signaling. HXK-dependent pathways of glucose signaling have more influence on the processes, such as seed germination, elongation of hypocotyl, flowering, leaf senescence, leaf and root growth, metabolism of carbon and nitrogen, infestation by pathogen, wounding, pigmentation, and eventual expression and repression of genes coupled with these processes. Lately, a conception is rising in which sugars such as sucrose, RFOs, and fructans, are identified as indirect contributors to antioxidative mechanisms and are furthermore concerned with direct ROS inactivation in different organelles, thus contributing to abiotic stress tolerance. In addition, an interaction between ROS and sugar signaling pathways points in the direction of sugars operating as an integrated molecule in cellular redox network. A broad molecular and physiological research is required to identify the route of sugar signaling involved in mediation of the processes initiating from embryogenesis and ending up with senescence. Sugar signaling has lately become the center of strong research efforts because of its role in all part of plant life cycle. Major effort should be contributed toward investigating the relations of sugars and phytohormones in controlling variety of processes including photosynthesis, carbon and nitrogen synthesis pathway, and growth and developmental responses. However, using specific sugars as osmoprotectants and/or antioxidants along with modulation of sugar metabolic enzymes is a promising tool for developing stress tolerant crops with improved yield and quality under challenging environmental conditions.

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References Almodares, A., Hadi, M., Dosti, B., 2008. The effects of salt stress on growth parameters and carbohydrates contents in sweet sorghum. Res. J. Environ. Sci. 2, 298 304. Amiard, V., Mueh, K.E., Demmig-Adams, B., Ebbert, V., Turgeon, R., Adams III., W.W., 2005. Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading. Proc. Natl. Acad. Sci. U.S.A. 102, 12968 12973. Amiard, V., Demmig-Adams, B., Mueh, K.E., Turgeon, R., Combs, A.F., Adams III., W.W., 2007. Role of light and jasmonic acid signaling in regulating foliar phloem cell wall in growth development. New Phytol. 173, 722 731. Anchordoguy, T.J., Rdolph, A.S., Carpenter, J.F., Crowe, J.H., 1987. Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24, 324 331. Anjum, S., Xie, X., Wang, L., 2011. Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agric. Res. 6, 2026 2032. Arabzadeh, N., 2012. The effect of drought stress on soluble carbohydrates (sugars) in two species of Haloxylon persicum and Haloxylon aphyllum. Asian J. Plant Sci. 11, 44 51. Arenas-Heurtero, F., Arroyo, A., Zhou, L., Sheen, J., Leon, P., 2000. Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6 reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev. 14, 2085 2096. Ashraf, M., Harris, P., 2013. Photosynthesis under stressful environments: an overview. Photosynthetica 51, 163 190. Ayala, A., Mun˜oz, M., Argu¨elles, S., 2014. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell Longev. 2014, 1 31. Barker, L., Kuhn, C., Weise, A., Schulz, A., Gebhardt, C., Hirner, B., et al., 2000. SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12, 1153 1164. Bernier, G., Havelange, A., Houssa, C., Petitjean, A., Lejeune, P., 1993. Physiological signals that induce flowering. Plant Cell 5, 1147 1155. Berthomieu, P., Conejero, G., Nublat, A., Brackenbury, W.J., Lambert, C., Savio, C., et al., 2003. Functional analysis of AtHKT1 in Arabidopsis shows that Na (1) recirculation by the phloem is crucial for salt tolerance. EMBO J. 22, 2004 2014. Boriboonkaset, T., Theerawitaya, C., Pichakum, A., Cha-um, S., Takabe, T., Kirdmanee, C., 2012. Expression levels of some starch metabolism related genes in flag leaf of two contrasting rice genotypes exposed to salt stress. Aust. J. Crop Sci. 6, 1579 1586. Borisjuk, L., Rolletschek, H., Walenta, S., Panitz, R., Wobus, U., Weber, H., 2003. Energy status and its control on embryogenesis of legumes: ATP distribution with in Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity. Plant J. 36, 318 329. Brun, T., Roche, E., Kim, K.H., Prentik, M., 1993. Glucose regulates acetyl CoA carboxylase gene expression in a pancreatic β-cell line (INS-1). J. Biol. Chem. 268, 18905 18911. Burke, J.J., 2007. Evaluation of source leaf responses to water-deficit stresses in cotton using a novel stress bioassay. Plant Physiol. 143, 108 121. Chandlee, J.M., 2001. Current molecular understanding of the genetically programmed process of leaf senescence. Physiol. Plant. 113, 1 8. Cheng, W.H., Endo, A., Zhou, I., Penney, J., Chen, H.C., Arroyo, A., et al., 2002. A unique short-chain dehydrogenase/reductase in Arabidopsis abscisic acid biosynthesis and glucose signalling. Plant Cell 14, 2723 2743. Courtois, B., Mclaren, G., Sinha, P.K., Prasad, K., Yadav, R., Shen, L., 2000. Mapping QTLs associated with drought avoidance in upland rice. Mol. Breed. 6, 55 66. Cowan, A.K., Freeman, M., Bjorkman, P.O., Nicander, B., Sitbon, F., Tillberg, E., 2005. Effects of senescenceinduced alteration in cytokinin metabolism on source-sink relationships and ontogenic and stress-induced transitions in tobacco. Planta 221, 801 814. Crowe, J., Crowe, L., Carpenter, J., Rudolph, A., Wistorm, C., Spargo, B., et al., 1988. Interactions of sugars with membranes. Biochim. Biophys. Acta 947, 367 384. Cuellar-Ortiz, S.M., DeLaPaz ArrietaMontiel, M., Acosta-Gallegos, J., Covarrubias, A.A., 2008. Relationship between carbohydrate partitioning and drought resistance in common bean. Plant Cell Environ. 31, 1399 1409.

Plant Life under Changing Environment

References

509

Cuoee, I., Sulmon, C., Gouesbet, G., Amrani, A., 2006. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J. Exp. Bot. 57, 449 459. Dai, N., Schaffer, A., Petreikov, M., Shahak, Y., Giller, Y., Ratner, K., et al., 1999. Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell 11, 1253 1266. Davenport, R.J., Munoz-Mayor, A., Jha, D., Essah, P.A., Rus, A., Tester, M., 2007. The Na(1) transporter AtHKT1;1 controls retrieval of Na(1) from the xylem in Arabidopsis. Plant Cell Environ. 30, 497 507. Davidson, A., Keller, F., Turgeon, R., 2011. Phloem loading, plant growth form, and climate. Protoplasma 248, 153 163. Dekkers, B., Schuurmans, J., Smeekens, S., 2004. Glucose delays seed germination in Arabidopsis thaliana. Planta 218, 579 588. Dielen, V., Lecouvet, V., Dupont, S., Kinet, J., 2001. In vitro control of floral transition in tomato (Lycopersicum esculentum Mill.) the model for autonomously flowering in plants using the late flowering uniflora mutant. J. Exp. Bot. 52, 715 723. Doorn, W., 2008. Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? J. Exp. Bot. 59, 1963. Eastmond, P., Graham, I., 2003. Trehalose metabolism: a regulatory role of trehalose-6-phosphate? Curr. Opin. Plant. Biol. 6, 231 235. Ehness, R., Ecker, M., Godt, D.E., Roitsch, T.H., 1997. Glucose and stress independently regulate source and sink metabolism and defence mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9, 1825 1841. Eveland, A., Jackson, D., 2011. Sugars, signalling and plant development. J. Exp. Bot. 63, 3367 3377. Fernandez, O., Bethencourt, L., Quero, A., Sangwan, R., Clement, C., 2010. Trehalose and plant stress responses: friend or foe? Trends Plant. Sci. 15, 409 417. Finkelstein, R., Lynch, T., 2000. Abscisic acid inhibition of radical emergence but not seedling growth is suppressed by sugars. Plant Physiol. 122, 1179 1186. Gamalei, Y.V., VanBel, A.J.E., Pakhomova, M.V., Sjutkina, A.V., 1994. Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplasmic minor-vein configuration. Planta 194, 443 453. Garg, A., Kim, J., Owens, T., Ranwala, A., Choi, Y., Kochian, L., et al., 2002. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc. Natl. Acad. Sci. U.S.A. 99, 15898 15903. Geigenberger, P., Reimholz, R., Geiger, M., Merlo, L., Canale, V., Stitt, M., 1997. Regulation of sucrose and starch metabolism in potato tubers in responsetoshort-term water deficit. Planta 201, 502 518. Gibson, S., 2005. Control of plant development and gene expression by sugar signaling. Curr. Opin. Plant. Biol. 8, 93 102. Gill, P., Sharma, A., Singh, P., Bhullar, S., 2003. Changes in germination, growth and soluble sugar contents of Sorghum bicolor (L.) Moench seeds under various abiotic stresses. Plant Growth Regul. 40, 157 162. Girousse, C., Bournoville, R., Bonnemain, J.L., 1996. Water deficit- induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol. 111, 109 113. Godt, D.E., Roitsch, T., 1997. Differential regulation of a tomato invertase gene family suggests an important function of extracellular isoenzymes in establishing and maintaining sink metabolism. Plant Physiol. 115, 273 282. Grata˜o, P., Polle, A., Lea, P.J., Azevedo, R.A., 2005. Making the live of heavy metal-stressed plants a little easier. Funct. Plant Biol. 32, 481 494. Hammond, J., Broadley, M., Bowen, H., Spracklen, W., Hayden, R., White, P., 2011. Gene expression changes in phosphorus deficient potato (Solanum tuberosum L.) leaves and the potential for diagnostic gene expression markers. PLoS One 6, 9. Harrington, N., Bush, D.R., 2003. The bifunctional role of hexokinase in metabolism and glucose signalling. Plant Cell 15, 2493 2496. Harvais, G., Hardley, G., 1967. The development of Orchis purpurella in asymbiotic and inoculated cultures. New Phytol. 66, 217 230. Hoekstra, F., Golovina, E., Buitink, J., 2001. Mechanisms of plant dessication tolerance. Trends Plant. Sci. 6, 431 438.

Plant Life under Changing Environment

510

19. The role of sugars in the regulation of environmental stress

Hoffmann-Thoma, G., VanBel, A.J.E., Ehlers, K., 2001. Ultra- structure of minor-vein phloem and assimilate export in summer and winter leaves of symplasmatically loading evergreens Ajuga reptans L., Aucuba japonica Thunb., and Hedera helix L. Planta 212, 231 242. Hofius, D., Hajirezaei, M.R., Geiger, M., Tschiersch, H., Melzer, M., Sonnewald, U., 2004. RNAi-mediated tocopherol deficiency impairs photo assimilate export in transgenic potato plants. Plant Physiol. 135, 1256 1268. Hu, M., Shi, Z., Zhang, Z., Zhang, Y., Li, H., 2012. Effects of exogenous glucose on seed germination and antioxidant capacity in wheat seedlings under salt stress. Plant Growth Regul. 68, 177 188. Huglin, P., 1986. Biologie et e´cologie de la vigne. INRA Payot Lausanne, Techniques and Documentation, Paris. Hummel, I., Pantin, F., Sulpice, R., Piques, M., Rolland, G., Dauzat, M., et al., 2010. Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol. 154, 357 372. Jang, J.C., Sheen, J., 1994. Sugar sensing in higher plants. Plant Cell 6, 1665 1679. Jang, J.C., Sheen, J., 1997. Sugar sensing in higher plants. Plant Cell 9, 5 19. Jang, J., Leon, P., Zhou, L., Sheen, J., 1997. Hexokinase as a sugar sensor in higher plants. Plant Cell 9, 15 19. Kaur, P., Gupta, A.K., Kaur, N., 2005. Embryo is not required for initiation of α-amylase activity in germinating cowpea seeds. Indian J. Biochem. Biophys. 42, 161 165. Knight, J.S., Gray, J.C., 1995. The N-terminal hydrophobic region of the mature phosphate translocator is sufficient for targeting to the chloroplast inner envelope membrane. Plant J. 7, 1421 1432. Koch, K., 2004. Sugar metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant. Biol. 7, 235 246. Krapp, A., Hofmann, B., Schafer, C., Stitt, M., 1993. Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for ‘sink regulation’ of photosynthesis? Plant Cell 3, 817 828. Krasensky, J., Jonak, C., 2012. Drought, salt and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593 1608. Lalonde, S., Boles, E., Hellmann, H., Barker, L., Patrick, J.W., Frommer, W.B., et al., 1999. The dual action of sugar carriers: transport and sugar sensing. Plant Cell 11, 707 726. Lebon, E., Pellegrino, A., Louarn, G., Lecoeur, J., 2006. Branch development controls leaf are a dynamics in grapevine (Vitis vinifera) growing in drying soil. Ann. Bot. 98, 175 185. Lecoeur, J., Wery, J., Turc, O., Tardieu, F., 1995. Expansion of pea leaves subjected to short water deficit: cell number and cell size are sensitive to stress at different periods of leaf development. J. Exp. Bot. 46, 1093 1101. Lemoine, R., Camera, S., Atanassova, R., De´dalde´champ, F., Allario, T., Pourtau, N., et al., 2013. Source-to-sink transport of sugar and regulation by environmental factors. Front. Plant Sci. 4, 1 21. Leopold, A.C., Sun, W.Q., Bernal-Lugo, L., 1994. The glassy state in seeds: analysis and function. Seed Sci. Res. 4, 267 274. Li, Y., Lee, K., Walsh, S., Smith, C., Handigham, S., Sorefan, K., et al., 2006. Establishing glucose and ABA regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using relevance vector machine. Genome Res. 16, 414 427. Liu, F., Jensena, C., Andersen, M., 2004. Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. Field Crops Res. 86, 1 13. Livingston, D., Hincha, D., Heyer, A., 2009. Fructan and its relationship to abiotic stress tolerance in plants. Cell. Mol. Life Sci. 66, 2007 2023. ¨ ., Sattelmacher, B., 2000. Solute balance of a Lohaus, G., Hussmann, M., Pennewiss, K., Schneider, H., Zhu, J.A maize (Zea mays L.) source leaf as affected by salt treatment with special emphasis on phloem retranslocation and ion leaching. J. Exp. Bot. 51, 1721 1732. Loreti, E., Bellis, L.D., Alpi, A., Perata, P., 2001. Why and how do plant cells sense sugars. Ann. Bot. 88, 803 812. Maeda, H., Song, W., Sage, T.L., Dellapenna, D., 2006. Tocopherols play a crucial role in low-temperature adaptation and phloem loading in Arabidopsis. Plant Cell 18, 2710 2732. Mahajan, N., Tuteja, S., 2005. Cold salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139 158. Mewis, I., Khan, M.A.M., Glawischnig, E., Schreiner, M., Ulrichs, C., 2012. Water stress and aphid feeding differentially influence metabolite composition in Arabidopsis thaliana (L.). PLoS One 7, 48661.

Plant Life under Changing Environment

References

511

Mittler, R., 2006. Abiotic stress, the field environment and stress combination. Trends Plant. Sci. 11, 15 19. Morita, A., Umemura, T., Kuroyanagi, M., Futsuhara, Y., Perata, P., Yamaguchi, J., 1998. Functional dissection of a sugar repressed a-amylase gene (Ramy1A) promotor in rice embryos. FEBS Lett. 423, 81 85. Nemati, I., Moradi, F., Gholizadeh, S., Esmaeili, M., Bihamta, M., 2011. The effect of salinity stress on ions and soluble sugars distribution in leaves, leaf sheaths and roots of rice (Oryza sativa L.) seedlings. Plant Soil Environ. 57, 26 33. O’Hara, L., Paul, M., Wingler, A., 2013. How do sugars regulate plant growth and development? New insight in to the role of trehalose-6-phosphate. Mol. Plant 6, 261 274. Ohto, M., Nakamura, K., 1995. Sugar-induced increase of calcium dependent protein kinases associataed with the plasma membrane in leaf tissues of tobacco. Plant Physiol. 109, 973 981. Ohto, M., Onai, K., Furukawa, Y., Aoki, E., Araki, T., Nakamura, K., 2001. Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol. 127, 252 261. Pattanagul, W., Thitisaksakul, M., 2008. Effect of salinity stress on growth and carbohydrate metabolism in three rice (Oryza sativa L.) cultivars differing in salinity tolerance. Indian J. Exp. Biol. 46, 736 742. Paul, M., Driscoll, S., 1997. Sugar repression of photosynthesis: the role of carbohydrate in signalling nitrogen deficiency through source: sink imbalance. Plant Cell Environ. 20, 110 116. Pego, J., Kortstee, A., Huijser, C., Smeekens, S., 2000. Photosynthesis, sugars and the regulation of gene expression. J. Exp. Bot. 51, 407 416. Pelleschi, S., Rocher, J.P., Prioul, J.L., 1997. Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant Cell Environ. 20, 493 503. Perata, R.T.N., Williamson, J.D., Conkling, M.A., Pharr, D.M., 1997. Sugar repression of mannitol dehydrogenase activity in celery cells. Plant Physiol. 114, 307 314. Prado, F., Boero, C., Gallardo, M., Gonzalez, J., 2000. Effect of NaCl on germination, growth and soluble sugar content in Chenopodium quinoa wild seeds. Bot. Bull. Acad. Sin. 41, 27 34. Price, J., Li, T., Kang, S.G., Na, J.K., Jang, J.C., 2003. Mechanisms of glucose signalling during germination of Arabidopsis. Plant Physiol. 132, 1424 1438. Price, J., Laxmi, A., Martin, S.K., Jang, J.C., 2004. Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16, 2128 2150. Rathinasabapathi, B., 2000. Metabolic engineering for stress tolerance: installing osmoprotectant synthesis pathways. Ann. Bot. 86, 709 716. Roitsch, T., 1999. Source-sink regulation by sugar and stress. Curr. Opin. Plant. Biol. 2, 198 206. Roitsch, T., Bittner, M., Godt, D.E., 1995. Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analogue and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol. 108, 285 294. Rolland, F., Winderickx, J., Thevelein, J.M., 2001. Glucose sensing mechanisms in eukaryotic cells. Trends. Biochem. Sci. 26, 310 317. Rolland, F., Moore, B., Sheen, J., 2002. Sugar sensing and signaling in plants. Plant Cell 14, 185 205. Rosa, M., Prado, C., Podazza, G., Interdonato, R., Gonzalez, J.A., Hilal, M., et al., 2009. Soluble sugars—metabolism, sensing and abiotic stress. Plant Signal. Behav. 4, 388 393. Sawhney, V., Singh, D., 2002. Effect of chemical desiccation at the post-anthesis stage on some physiological and biochemical changes in the flag leaf of contrasting wheat genotypes. Field Crop Res. 77, 1 6. Schrier, A., Hoffmann-Thoma, G., VanBel, A.J.E., 2000. Temperature effects on symplasmic and apoplasmic phloem loading and loading associated carbohydrate processing. Aust. J. Plant. Physiol. 27, 769 778. Sheen, J., 1990. Metabolic repression of transcription in higher plants. Plant Cell 2, 1027 1038. Singh, M., Kumar, J., Singh, S., Singh, V., Prasad, S., 2015. Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev. Environ. Sci. Bio/Technol. 14, 407 426. Smeekens, S., 2000. Sugar induced signal transduction in plants. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 52, 49 81. Smeekens, S., Ma, J., Hanson, J., Rolland, F., 2010. Sugar signals and molecular networks controlling plant growth. Curr. Opin. Plant. Biol. 13, 274 279. Sonnewald, U., Brauer, M., Schaewen, A., Stitt, M., Willmitzer, L., 1991. Transgenic tobacco plants expressing yeast-derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions. Plant J. 1, 95 106.

Plant Life under Changing Environment

512

19. The role of sugars in the regulation of environmental stress

Suwa, R., Fujimaki, S., Suzui, N., Kawachi, N., Ishii, S., Sakamoto, K., et al., 2008. Use of positron-emitting tracer imaging system for measuring the effect of salinity on temporal and spatial distribution of 11C tracer and coupling between source and sink organs. Plant Sci. 175, 210 216. Tegeder, M., Wang, X.D., Frommer, W.B., Offler, C.E., Patric, J.W., 1999. Sucrose transport into developing seeds of Pisum sativum L. Plant J. 18, 151 161. Trouverie, J., Chateau-Joubert, S., Thevenot, C., Jacquemot, M.P., Prioul, J.L., 2004. Regulation of vacuolar invertase by abscisic acid or glucose in leaves and roots from maize plantlets. Planta 219, 894 905. Turgeon, R., 2010. The puzzle of phloem pressure. Plant Physiol. 154, 578 581. VanBel, A.J.E., Gamalei, Y.V., 1992. Ecophysiology of phloem loading in source leaves. Plant Cell Environ. 15, 265 270. Wani, A., Ahmad, A., Hayat, S., Fariduddin, Q., 2013. Salt-induced modulation in growth, photosynthesis and antioxidant system in two varieties of Brassica juncea. Saudi J. Biol. Sci. 20, 183 193. Westgate, M.E., Schussler, J.R., Reicosky, D.C., Brenner, M.L., 1989. Effect of water deficits on seed development in Soybean: II. Conservation of seed growth rate. Plant Physiol. 91, 980 985. Wingler, A., Purdy, S., MacLean, J., Pourtau, N., 2006. The role of sugars in integrating environmental signals during the regulation of leaf senescence. J. Exp. Bot. 57, 391 399. Wingler, A., Dellate, T., O’Hara, L., Premavesi, L., Jhurreea, D., Paul, M., et al., 2012. Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol. 158, 1241 1251. Xiao, W., Sheen, J., Jang, J.C., 2000. The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol. Biol. 44, 451 461. Xu, S.M., Liu, L.X., Woo, K.C., Wang, D.L., 2007. Changes in photosynthesis, xanthophyll cycle and sugar accumulation in two North Australia Tropical species differing in leaf angles. Photosynthetica 45, 348 354. Xu, Z., Jiang, Y., Zhou, G., 2015. Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Front. Plant Sci. 6, 701. Yang, J., Zhang, J., Wang, Z., Zhu, Q., Liu, L., 2002. Abscisic acid and cytokinins in the root exudates and leaves and the relationship to senescence and remobilization of carbon reserves in rice subjected to water stress during grain filling. Planta 215, 645 652. Yang, J., Zhang, J., Wang, Z., Xu, G., Zhu, Q., 2004. Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiol. 135, 1621 1629. Yaseen, M., Ahmad, T., Sablok, G., Standardi, A., Hafiz, I., 2013. Review: role of carbon sources for in vitro plant growth and development. Mol. Biol. Rep. 40, 2837 2849. Yuanyuan, M., Yali, Z., Jiang, L., Hongbo, S., 2009. Roles of plant soluble sugars and their responses to plant cold stress. Afr. J. Biotechnol. 8, 2004 2010. Zhu, G., Ye, N., Zhang, J., 2009. Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol. 50, 644 651.

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20 Proteomics in relation to abiotic stress tolerance in plants Arti Gautam, Poonam Pandey and Akhilesh Kumar Pandey Department of Biochemistry, Institute of Science, Banaras Hindu University, Varanasi, India

20.1 Introduction Plants constantly face adverse environmental conditions, which include a number of abiotic stresses, such as temperature extremities such as heat and cold, flood, salinity, drought, and metal toxicity, which adversely influence growth, metabolism, and hence the yield of crops (Hasanuzzaman et al., 2013). Recent advances in molecular biology and proteomics have provided a deeper insight into understanding the roles of various metabolic pathways, proteins, enzymes associated with adaptation and tolerance of plants to various abiotic stresses (Srivastava et al 2013; Pandey et al., 2019). Plants adapt to adverse effects of stresses by inducing changes in the expression of genes leading to alterations in the abundance of proteins (Gong et al 2015; Pandey et al., 2019). Response to stress involves mainly three groups of genes that play an important role in signaling cascades, protection of membranes and other genes/proteins associated with uptake, and transport of ions and water molecules (Rout and Panigrahi, 2015; Pandey et al., 2019). In order to perform these vital processes, plants rely on a variety of posttranslational modifications and oxidative modifications of side chains of various amino acid residues (Mock and Dietz, 2016). Reactive oxygen species (ROS) overproduced under abiotic stresses induce numerous posttranslational modifications such as phosphorylations (Durcan and Fon, 2015), glycosylations (Catala´ et al., 2011), acetylations (Nallamilli et al., 2014), and succinylations (Zhang et al., 2011). Acetylation and deacetylation events perform crucial roles in regulation of gene expression (Catala´ et al., 2011). Extent of histone acetylation is maintained by histone acetyltransferase (HAT) and histone deacetylase (HDAC) (Hou et al., 2015). Histone proteins undergo various modification processes such as methylation, acetylation, ubiquitination, sumoylation, phosphorylation, and ribosylation (Luo et al., 2012). These events play crucial roles during stressful conditions. On the other hand the tubulin proteins, which have fundamental role in maintaining the dynamic structures within the plant cell,

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also bear multiple modification sites (Cosgrove, 2015). Tubulins play an important role in tubular reorganization on stress perception (Ban et al., 2013). ROS cause reversible and irreversible modifications in proteins that alter the regulation of plant metabolism (Nallamilli et al., 2014). ROS mediate rapid systemic signaling and modifications caused by them to regulate the signal cascades and metabolic pathways (Miller et al., 2009). Recent studies on the role of ROSmediated protein modification include sulfonylation (Kang et al., 2018), glutathionylation (Ullevig et al., 2016), tryptophan oxidation (Gao et al., 2016), carbonylation (Matamoros et al., 2018), and nitrosylation (Mata-Pe´rez and Spoel, 2019), which affect the transcriptional regulatory networks and hence gene expression during abiotic stresses (Ohama et al., 2017). Besides, different phytohormones, such as auxins (Tognetti et al., 2010), gibberellins (Colebrook et al., 2014), abscisic acid (ABA) (Boursiac et al., 2013), and brassinosteroids (Xia et al., 2009), also mediate plant-defense response on exposure to abiotic stresses. Auxin regulates plant development (Tognetti et al., 2012) while gibberellic acid and abscisic-acid crosstalk is responsible for seed dormancy and embryogenesis (Boursiac et al., 2013). Hence, signaling interactions between different phytohormones affect growth. These interactions coordinate different genes along with their regulators associated with stress tolerance. Plant growth and development processes are highly affected by ubiquitins that regulate protein stability. Intensive efforts have been made to identify the E3 ligases that modulate stress-responsive transcription factors and facilitate response to abiotic stresses (Ling and Jarvis, 2015). Ubiquitin, which is an 8 kDa highly conserved protein, covalently binds to other proteins so as to regulate the stability and functions of the proteins (Vierstra, 2009). Protein-modification process via ubiquitination has been regarded as a prominent mechanism in stress tolerance (Guo et al., 2008). The role of secondary messengers, such as Ca21, and its sensing proteins, such as calmodulin (CaM), is associated with the transduction of Ca21 signals (Reddy et al., 2011). CaM after interacting with Ca21 leads to altered conformation and affects the activity of other CaM-binding proteins (Astegno et al., 2017). The CaM-binding proteins play an important role in stress response in plants (Yadav et al., 2018). Proteome analysis has helped in a long way to identify the wider range of proteins that are associated in various ways in providing protection against different environmental stresses in plants (Budak et al., 2015). To ensure sustainable production of crops and to accomplish the guarantee of food for the rising global population, it is imperative to produce stress-tolerant crop species with inherent mechanisms to ensure cellular defense under unfavorable stressful conditions (Martinez et al., 2018; Pandey et al., 2019). These mechanisms include perception of stresses, signaling mechanism, transcriptionally inducing stressregulating genes followed by generation of the stress-associated proteins (Verma et al., 2016). Novel genes and biochemical pathways that assist plants in adapting to the adverse conditions have been widely studied (Petrov et al., 2015). This chapter updates and summarizes our present status of knowledge related to proteomics approaches, roles of wide range of proteins, and associated mechanisms in relation to enhancing stress tolerance in crops.

20.2 Understanding and identifying key metabolic proteins associated with abiotic stresses Adverse environmental conditions negatively influence crop growth and yield and threaten food security (Lake et al., 2012). Key adverse environmental conditions, which are Plant Life under Changing Environment

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regarded as abiotic stress, include temperature extremities (heat and chilling), drought, deprivation of nutrients, radiations, excessive levels of metals in the soil such as cadmium, lead, aluminum, arsenate, and chromium (Ashraf, 2014). Cell survival under abiotic stress mainly depends on cell adaptation to the environment. The adaptation and corresponding tolerance mechanisms of plants to stresses have been much studied during the past many years (Shelden et al., 2013; Ahmed et al., 2012; Srivastava et al., 2013; Emon, 2016). Difference gel electrophoresis, which is a useful technique for protein labeling and separations, along with mass spectrometry have helped researchers in studying alterations in protein abundance due to stress and to separate one particular protein from its isoforms (Ahsan et al., 2010). Tools of bioinformatics are applied in identifying gel spot patterns and physiological states (Hwang et al., 2012). These recent advances have provided a deep insight in studying the proteins and corresponding mechanisms involved in stress response. Cellular defense mechanism mainly involves expression of associated genes and the corresponding proteins. Three major groups of genes, involved in the stress response, are as follows: 1. Genes that play role in signaling cascades and are associated with transcriptional regulation (Miller et al., 2010). 2. Genes that have a role in the protection of membranes and proteins (Khan et al., 2015a,b). 3. Genes that are involved in uptake and transport of ions and water molecules (Wu et al., 2015).

20.2.1 Proteins and genes associated with signaling cascades and transcriptional regulation C-repeat/Drought-responsive element-binding (DREB) factor is a major transcriptional factor gene expressed under cold stress through C-repeat binding factor (CBF) dependent as well as independent transcriptional pathway (Riechmann et al., 2000). Being an important transcription factor, DREB works in an ABA-dependent and -independent way and interacts with the cis-element of promoter area of different genes associated with stressful conditions (Singh and Laxmi, 2015). The CBF cold-responsive route is maintained in many species of plants (Lee and Seo, 2015). DREB homologous genes are present in many plants such as Arabidopsis, maize, rye, wheat, sorghum, rice and perennial rye grass (Rehman and Mahmood, 2015). WRKY proteins are other transcription-factor genes, which are associated with plant signaling in response to abiotic stress (Kume et al., 2005). WRKY factors maintain the expression of different stress-related genes, which thereby induces tolerance to abiotic stress (Banerjee and Roychoudhury, 2015). The WRKY genes are reported to provide tolerance against different types of abiotic stresses along with playing a key role in conferring interplay of biotic and abiotic stress (Rushton et al., 2010). WRKY genes that are reported in many plant species, such as Arabidopsis (74 genes), rice (over 100 genes), soybean (197 genes), Selaginella moellendorffii (35 genes), papaya (66 genes), Pinus (80 genes), poplar (104 genes), Physcomitrella patens (38 genes), sorghum (56 genes), Ricinus communis (56 genes), barley (45 genes), Cucumis sativus (55 genes), have been identified (Kunkel and Brooks, 2002; Singh et al., 2002; Mahalingam et al., 2003; Katagiri, 2004; Liang et al., 2015). Late embryogenesis abundant (LEA), which is a functional protein, and the proteins that

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are involved in osmoprotectant biosynthesis provide protection to environmental stresses, such as drought, chilling, and salinity, while regulatory proteins, such as DREB, abscisic acid-responsive elements and NAM, ATAF and CUC (NACs), are crucial for the induction of functional proteins (Wang et al., 2019). Some phytohormones, such as ABA, which regulate stomata aperture, seed dormancy, and vegetative growth, are known to be associated with stress-response mechanism and thus have been considered as stress hormone (Rushton et al., 2010). At the onset of drought or salinity the ABA-responsive genes are triggered, which results in quick closure of stomatal aperture along with osmoprotectant synthesis (de Zelicourt et al., 2016). Recently in a study, some genes that induce stress, such as those responsive to dehydration (RD), early-responsive to dehydration, coldregulated, and cold-inducible families, are reported in Arabidopsis (Lee and Seo, 2015).

20.2.2 Proteins and genes with roles in the protection of membranes The chaperon proteins associated with membrane are implicated in many physiological events inside the cells. Certain heat shock proteins (HSPs) maintain the stability of membrane by maintaining its fluidity and restoring the membrane functionality during stress (Usman et al., 2015). LEA proteins, which are known to be highly hydrophilic, accumulate during salinity, low temperature, and drought and water deficit. Analysis of the LEA proteins revealed seven different forms (LEA1
LEA7) (Banerjee and Roychoudhury, 2016). Membrane stabilization is reported to be one of the major functions attributed to these proteins because LEA proteins have been found associated with anionic phospholipids vesicle and maintain membrane structure under freezing temperatures (Hara et al., 2012). Further, many studies report transcription of ZmLEA3, which was due to low temperature and osmotic stress in tobacco (Janmohammadi et al., 2015). Many scientists have been studying the important role of plasma membrane in providing stress tolerance in plants (Li et al., 2014; Mickelbart et al., 2015; Hong et al., 2018). Duan et al. (2012) have identified eight plasma membrane
associated proteins in rice roots, which respond to salt stress. These proteins include proton ATPase regulators as well as pH-regulatory proteins (Boudet et al., 2006). Later, 18 salt responsive proteins were identified (Aghaei et al., 2009). The proteomic analysis confirmed that the presence of leucine-rich-repeat type receptorlike proteins accumulated in cortex plasma membrane are showing response against salt stress in plants (Nohzadeh, Malakshah et al., 2007). Further, Kawamura and Uemura (2003) reported changes in the level of 38 proteins associated with plasma membrane after cold-stress treatment in Arabidopsis. These include dehydration proteins along with a newly identified cold stress
induced protein, plant synaptotagmin 1 that was also investigated, which is involved in repairing the plasma membrane during its disruption of freeze-thaw cycle. Many researchers have reported that cyanobacteria histidine kinase Hik33 and the Bacillus subtilis histidine kinase DesK perform crucial role in regulating gene expression under chilling conditions, while the compatible osmolytes and antioxidants are produced by mitogen-activated protein kinase (MAPK) pathways in yeast and animals (Zhu, 2016). A thorough study for understanding the relationship of histidine kinases and MAPK pathways in osmotic stresses will certainly help in investigating the signal mechanism during osmotic stress (Sreenivasulu et al., 2007).

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20.2.3 Proteins involved in water and ion uptake and transport During salinity stress, plants need to maintain a redox balance, which involves Na1 and Cl2 uptake along with proper compartmentalization of the toxic ions inside the vacuoles without accumulating them in soil (Khare et al., 2015). Na1 and Cl2 are normally present in vacuoles and are parallelly adjusted by the osmolytes, which include proline, sorbitol, mannitol, and glycinebetaine (Sharma, 2016). Plants facing salt stress can accumulate more Na1 and Cl2 ions, which affect its physiology (Al Hassan, 2018). The vacuolar H1-ATPase and the H1-pyrophosphatase generate an electrochemical gradient of protons, which drives the Na1/H1 antiporter that regulates Na1 sequestration into the vacuole (Yin et al., 2015). Sodium extrusion from the root
soil interface is critical for tolerance to salinity (Sze and Chanroj, 2018). Na1 efflux protein, located at the plasma membrane, is the only Na1/H1 antiporter that maintains salt tolerance inside the plant system (Zhu et al., 2015). Vacuolar antiporter Na1/H1, antiporter AtNHX1, and the plasma membrane K1/Na1 symporters are characterized, which provided important basis of tolerance toward the salt stress (Sze and Chanroj, 2018). Studies on Cl2 transporters are aimed at voltage-dependent chloride channel family and cation chloride cotransporters, which encode 1 and 2 genes in Arabidopsis and rice, respectively (Zhang et al., 2018). Aquaporins present in plasma membrane are responsible for drought tolerance in plants due to its well-known role in transport activities of small and uncharged solutes (Zargar et al., 2017). It regulates dynamic changes in root, stem, and leaf hydraulic conductivity mediated by PIPs (plasma membrane
intrinsic proteins), TIPs (tonoplast-intrinsic proteins) present in plasmalemma and tonoplast of the plant cells, respectively (Pou et al., 2013), small basic intrinsic proteins, Nodulin 26-like intrinsic proteins, and X-intrinsic proteins, which are other subgroups of aquaporins (Huang et al., 2006). Water uptake in roots mainly occurs by PIPs and TIPs, which are reported to be expressed during drought stress, which hereby suggests its major role in stress acclimation. In a study done by Byrt et al. (2007), the expression of AtPIP2;3 was found to be increased during drought, suggesting a major role of aquaporins, while other studies reported the expression of 35 aquaporin homologs in Arabidopsis thaliana on exposure to drought only (Khan et al., 2015a,b). High expression of most of the PIP and some TIP genes was also reported in the same study (Maurel et al., 2015; Fox et al., 2017; Sonah et al., 2017).

20.3 Effect of reactive oxygen species on protein modification Protein oxidative modifications or protein oxidation is due to the interaction of protein residues with ROS and reactive nitrogen species (RNS) (Waszczak et al., 2015). Mitochondria is a major ROS production site, but many enzymes, such as α-ketoglutarate dehydrogenase complex, nicotine adenine dinucleotide phosphate (NADPH) oxidase, d-amino acid oxidases, dihydrolipoamide dehydrogenase, and xanthine oxidase, are also involved in producing ROS (Verma et al., 2016). These protein modifications not only change the cellular redox state but also protect the target proteins from further damages (Espinosa-Diez et al., 2015). Recent researches have highlighted some important

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posttranslational modifications such as phosphorylation, glycosylation, acetylation, and succinylation (Waszczak et al., 2015; Aroca et al., 2015; Friso and van Wijk, 2015). Cysteine residues of protein undergo reversible redox modifications, such as sulfonylation, carbonylation, glutathionylation and, S-nitrosylation, which are discussed as follows.

20.3.1 Posttranslational modifications 20.3.1.1 Phosphorylation Protein phosphorylation takes part in regulatory mechanisms in plants under abiotic stress as it is able to change protein stability, activity, and interaction mechanism with several other proteins (Sanyal et al., 2016). Phosphorylation of proteins regulates several developmental phenomena such as growth, metabolism, apoptosis including stress response (Zo¨rb et al., 2010). Therefore stress due to phosphorylation of protein can retard the growth of the plant and hence influence the productivity (Fig. 20.1). The crops including maize, sugar beet and wheat have been studied under salt stress and it was found that the process of phosphorylation takes place in hydroxylated amino acid such as (S), threonine (T), and Y residues (Yu et al., 2016). Protein kinases and phosphatase are reported to be associated with regulation of phosphorylation in different crops including wheat and maize (Ma et al., 2018; He et al., 2015). Protein kinase mediates the addition of phosphate group on amino acid residue of the protein (Kumar et al., 2014). DSP4 gene showed upregulated expression under cold stress in chestnut suggesting a phosphorylated mediated mechanism to tolerate the stress (Chao et al., 2016). MAPKs belong to the group of protein kinase, which phosphorylates serine or threonine residue of the target protein and alters the corresponding

Environmental stress

Increased ROS

Transcription factors Signaling

Posttranslational modification Protein

cascades MAPK

Phosphorylation

Protein kinases

Calnexin

Glycosylation

Calreticulin/HSP

Enhanced High temperature/ Salt/Drought/cold stress

FIGURE 20.1

tolerance

Altered protein structure/functions

Heavy-metal stress, Nutrient deficiency

KAT/KDAC

Succinyl-CoA

Acetylation

Succinylation

An overview of protein-modification processes induced by abiotic stresses in crop plants.

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functions (Miller and Turk, 2018). MAPK pathway was identified in rice plants, which acts against drought, and osmotic and saline conditions (Kazan, 2015). Another gene, ATMPK3, that encodes the Arabidopsis MAPK is reported to express in cold, drought, salt, and touch stress
exposed plants (Wimalasekera and Scherer, 2018). calcium-dependent protein kinases (CDPKs) are the serine/threonine protein kinases that are implicated in defense to cope with cold, salt, and drought in maize and Arabidopsis (Forni et al., 2017). In this way, protein kinases are involved in regulating the phosphorylation and signal-transduction processes. 20.3.1.2 Glycosylation Glycosylation is one of the important protein-modification processes, which include aspartate or S/T or Y residues targeted N- and O-glycosylations, respectively (Baker et al., 2016). It plays a role in protein folding, protein stability, and protein
protein interaction (Fig. 20.1) (Mustafa and Komatsu, 2014). The glycosylation process is followed by protein folding, which involves the role of calreticulin, calnexin, and heat-shock proteins (Baker et al., 2016). More than a thousand N-glycosylated proteins were identified in model plant A. thaliana (Reis et al., 2016). Many eukaryotic proteins are reported to be glycosylated and take part in a number of physiological processes (Fu et al., 2016). The N-linked glycans regulate the biological activities of proteins, induce correct folding, and confer prevention to proteolytic degradation (OliveiraFerrer et al., 2017). Biosynthesis of these N-linked glycans occurs in endoplasmic reticulum, and ER is also involved in various cellular processes such as protein synthesis, transfer, and degradation (Harmoko et al., 2016). Flooding stress causes negative effects on ER as it affects the process of glycosylation (Mega, 2005). The differential analysis revealed changes in abundance of 69 glycoproteins within 2 days of flooding stress in soybean roots (Zhang et al., 2016). Due to the influence of salt stress in tomato plant, the HSPs were overexpressed, which resulted in protein folding and thus rescued from cellular damages (Fu et al., 2016). 20.3.1.3 Acetylation The abiotic stress causes acetylation of histone and nonhistone proteins under physiological stress (Li et al., 2014). Mass spectrometry and chromatin immunoprecipitation techniques revealed the presence of 28 histone-modification sites in Arabidopsis. The acetylation process of proteins usually takes place in two different forms: reversible and irreversible (Baeza et al., 2016). Irreversible protein acetylation includes modification of Nα-terminal by Nt-acetyltransferase, while reversible ε-amino group modification includes modification of lysine (K) by K acetyltransferases and K deacetylases (Xiong et al., 2016). Several studies have shown that the process of acetylation causes metabolic process, signal transduction, protein translation, and RNA processing (Nallamilli et al., 2014; SmithHammond et al., 2014; Zhong et al., 2013; Komatsu et al., 2011). In a study with rice, 44 acetylated proteins were identified, which were involved in cell death process (SmithHammond et al., 2014). After studying acetylated proteins in wheat, a total of 277 proteins were identified to be involved in maintaining a balance of energy production during stress conditions (Komatsu et al., 2011). Acetylation of proteins modifies the nonhistone metabolic enzymes and changes gene expression (Zhong et al., 2013) (Fig. 20.1). According to one study, the rice HDAC, OsSRT1, was reported to enhance the expression of the metabolic processes associated with genes. Similarly, a drought-exposed Arabidopsis plant

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showed acetylation (
CH3) of histone proteins H3 Lys23 (H3K23ac) and histone H3 Lys27 (H3K27ac) (He et al., 2016). In another study with rice plants, the level of H3K4me3 was increased when the plants were exposed to submergence treatment (Zhen et al., 2016). This shows the gradual increase of histone H3 acetylation due to submergence treatment. 20.3.1.4 Succinylation Succinylation, involved in various metabolism regulations, such as tricarboxylic acid cycle, is the addition of succinyl group to a lysine residue of a protein molecule (He et al., 2016). It is widely reported in prokaryotes as well as eukaryotes. Lysine acetylation and succinylation shows the functional interaction and crosstalk to carry out the various metabolic processes (Zhang et al., 2011). Succinylated proteins take part in different metabolic processes such as glycolysis/gluconeogenesis, citrate cycle, carbon fixation, and ribosome (Zhen et al., 2016). Lysine acetylation and succinylation were studied in germinating rice seedlings and 389 acetylated and 261 succinylated proteins were identified (Jin and Wu, 2016). Many researchers studied succinylation process and reported different target sites for succinylation present on histone H3 (K14, K56, K79, and K122) in tomato plant (He et al., 2016). Brachypodium distachyon also reported to exhibit succinylation-associated protein modification in carbon-metabolism pathways (Jin and Wu, 2016).

20.3.2 Other posttranslational modifications of crop proteins 20.3.2.1 Histone Gene expression is also dependent upon packaging of DNA with histones. Plants regulate the expression of genes to cope with the stressful conditions (Luo et al., 2012). Modification of histone proteins such as H3K9ac, H3K23ac, H3K27me3, H3K4me3, H3K9me2, H3K27ac, and H4ac, together with DNA methylation are reported in recent studies (Neumann et al., 2016). Mass spectrometry and biochemical assays have helped scientists in identifying the histone-modification sites (Luo et al., 2012). Processes of acetylation, methylation, phosphorylation, ubiquitination, and succinylation are regulated by histone variants as studied in tomato and other crops by many researchers (Sanei et al., 2010; Zhen et al., 2016; He et al., 2016; Mahrez et al., 2016). The phytohormone gibberellin promotes acetylation of histone, while another phytohormone ABA suppresses acetylation (Rodrı´guez-Sanz et al., 2014). Eukaryotic gene activity is dependent on histone modifications to a very large extent (Sanei et al., 2010). CHIP assay studies have revealed that drought exposure alters H3 N tail and modifies the associated gene activity (Li et al., 2014). Enzymes associated with histone modifications, such as HAT, HDAC, histone methyltransferase, and histone demethylase, take part in modifying the N-terminal tails of histones (Aiese Cigliano et al., 2013) (Fig. 20.2). Histone proteins are built up of basic amino acids such as arginine and lysine. These basic residues undergo covalent modifications by methylation, acetylation, phosphorylation, and ubiquitination (Li et al., 2014). The HAT acetylates the lysine residues present on histone N tails (Sanei et al., 2010). AtGCN5 is the most studied HAT protein that interacts with the transcriptional adapter proteins and has the ability to alter the gene expression

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FIGURE 20.2 Regulation of expression of genes by histone modification induced by abiotic stress.

during cold and light stress (Mahrez et al., 2016). The linker histone or H1 is reported to be a very important molecule that affects the gene activity. Three linker histone H1 homologs were reported in Arabidopsis, and HIS1
3 gene expression was induced on exposure to drought (Mahrez et al., 2016). Moreover, the expression of H3K4me3 and H3K9ac proteins were also induced on drought stress, and its production was decreased under nondrought conditions (Hou et al., 2015). Exposure to salt stress induces histones modifications by the process of methylation, acetyletion and phophorylation while heat stress leads to sumoylation of histones proteins (Neumann et al., 2016). 20.3.2.2 Tubulin An increase in the level of protein tubulin in African as well as in Asian rice cultivars has shown its role in tolerance toward salt stress (Ban et al., 2013). Due to its dynamic structure, the microtubules play an important role in cell morphogenesis and contribute not only in mitotic spindle and cell-plate formation but also in cell growth, intracellular transport, and cell-wall deposition (Ban et al., 2013). Possessing a very simple structure, microtubules can precisely regulate the cell cycle and the cell-differentiation process. Presence of multiple modification sites allows different pathways of stress regulation including tyrosination, phosphorylation, acetylation, and polyglutamylation (Gzyl et al., 2015). Posttranslational modification occurs at C-terminal tails of both α and β subunits. In the process of detyrosination, the C-terminal amino acid tyrosine is enzymatically removed and detyrosinated tubulin is formed, which hinders the process of depolymerization (Wang et al., 2004). Thus the normal process of growth and development is altered (Fig. 20.3). Acetylation causes the addition of acetyl group to α-amino group of lysine 40

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FIGURE 20.3 Presence of multiple modification sites at C-terminal tail of tubulin proteins, which allow regulation of abiotic stress tolerance in plants.

and alters the normal functioning of tubulin proteins (Wang et al., 2004). Addition of glutamate to the C-terminal tails of either of α- or β-tubulins causes modification in the microtubule and the corresponding process is polyglutamylation (Huang and Lloyd, 1999). In a study, Cd toxicity alters the level of tyrosinated/detyrosinated, acetylated, and polyglutamylated isoforms of tubulin in root tips of soybean (Ban et al., 2013). During hyperosmotic stress, α-tubulin undergoes phosphorylation and promote the depolymerization of microtubules in rice; thus plant physiological status is changed (Gzyl et al., 2015). During drought stress, the ubiquitin-dependent proteolysis regulated the tubulin complex
related serine/threonine protein kinase named OsNek6 to combat the stressful conditions (Liu et al., 2015). Various researches have proved that microtubules rebuild its structure in response to external stimuli.

20.3.3 Reactive oxygen species
induced protein oxidative modifications ROS is known to induce reversible and irreversible alterations in protein structure, which results in the activation of transcriptional regulatory networks. Worldwide attention has been given to ROS-induced protein alterations to increase our fundamental understanding of expression and regulation of genes during abiotic stress in different plants. The most important posttranslational modifications induced by ROS are sulfonylation, carbonylation, glutathionylation, and S-nitrosylation (Fig. 20.4). 20.3.3.1 Sulfonylation Sulfonylation is considered to be an important process that affects the activity of many enzymes as it involved in the oxidation of sulfhydryl groups, which results in the formation of disulfide bridges between cysteine residues (Choudhury et al., 2017). It is crucial

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523 FIGURE 20.4 Protein oxidative modification and regulation of protein stability in abiotic stress
induced plants.

for cell growth and development because the oxidation process leads to change in the conformation of protein and alters its activity (Reczek and Chandel, 2015). To regulate the toxicity a redox homeostasis process takes place in which protein is recovered from its oxidized state via peroxiredoxins, thioredoxins, and the glutathione (GSH) system (Netto and Antunes, 2016). Sulfonation is another biological phenomenon reported in various organisms in which sulfotransferase enzyme transfers the sulfonate group from the donor 30 -phosphoadenosine 50 -phosphosulfate to an appropriate acceptor and thus regulates the physiological process (Speiser et al., 2018). Sequence analyses have revealed the presence of 18 and 35 cytosolic sulfotransferases in Arabidopsis and rice, respectively (Gustavsson et al., 2002). Abiotic stresses and hormone treatments promote AtSOT12 gene expression in Arabidopsis indicating the role of sulfonation of small molecules in stress and hormone response (Chen et al., 2015). 20.3.3.2 Glutathionylation Under stressful conditions, proteins undergo the oxidation of cysteine residues to form cysteine sulfenic acid and cysteine sulfinic acid through reversible and irreversible process, respectively (Kumar et al., 2010). The process of S-glutathionylation occurs when the sulfenic acid reacts with GSH, which is a low molecular-weight tripeptide thiol. This process is also important for buffering oxidized glutathione (GSSG)/GSH pool during redox homeostasis under the stressful conditions (Csisza´r et al., 2018). GSH, a low molecularweight tripeptide thiol, plays a very important role in the oxidative signaling of GSHrelated enzymes (Zaffagnini et al., 2012). It scavenges the ROS by GSH-ascorbate cycle. Plant possesses GSH or GSH homolog, in which the amino acid such as serine, β-alanine, or glutamate replaces the glycines, which is a C-terminal amino acid. GSH is synthesized

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in ATP-dependent manner and γ-glutamylcysteine mediated by γ-glutamyl synthetase enzyme is formed in cytosol, chloroplast, and mitochondria followed by the addition of glycine to γ-glutamylcysteine to synthesize GSH (Kumar et al., 2010). Drought-exposed Vigna radiata showed a decreased level of γ-glutamylcysteine synthetase activity (Nahar et al., 2016). The level of GSH maintains a reduced environment inside the cell and normally GSH to GSSG ratio is 20:1 but during stress, the ratio shifts toward GSSG (Mortimer et al., 2008). A comparative study between sensitive and tolerant plants has shown high GSH:GSSG ratio in tolerant species and low GSH:GSSG ratio in sensitive varieties (Zaffagnini et al., 2012). As stated before, cysteine residues undergo oxidation to form cysteine sulfenic acid and sulfinic acid, which results in altered conformation of the corresponding protein and finally its degradation (Kumar et al., 2010). Glutathionylation of these proteins by GSSG leads to their temporary protection. Contribution of glutathionylation in providing tolerance was confirmed by a study in which the fluctuation of water content in plants was accompanied by their equal change in cellular redox state (Stro¨her et al., 2016). 20.3.3.3 Tryptophan oxidation The tryptophan biosynthetic pathway is responsible for the generation of different secondary metabolites in the plant system. These secondary metabolites are well known for their prominent role in protein synthesis (Gray and Winkler, 2015). ROS can also modify the tryptophan by oxidizing it to Trp hydroperoxide, which then decomposes to N-formylkynurenine and kynurenine as major end products (Ehrenshaft et al., 2015). These end products are reported to take part in the regulation of photosynthesis. Oxidation of TRP356 to NFK takes place on exposure to high light stress as well as increased photo inhibition inside the CP43 subunit of PSII (Choudhury et al., 2017). Response of tryptophan pathway was studied for amino acid
deprivation condition, and accumulation of indolic phytoalexin camalexin was reported (Gray and Winkler, 2015; Ehrenshaft et al., 2015). These results clarify that on starvation, the biosynthesis of secondary metabolites is induced, which is regulated by Trp pathway (Gray and Winkler, 2015). 20.3.3.4 Carbonylation Carbonylation is an irreversible protein oxidation, such as that of His, Arg, Pro, Lys, and Thr residues, which alters the activity of several enzymes in mitochondria involving pyruvate dehydrogenase, aconitase, and glycine decarboxylase. This includes introduction of reactive carbonyl group on amino acid residues of the target proteins (Shannon and Weerapana, 2015). These proteins or enzymes are involved in different metabolic processes, and therefore the inhibition of these enzymes alters the TCA cycle and results in the reduction of level of energy status inside the cell (Madian and Regnier, 2010). ROS, such as O22, H2O2, and OH, have the ability to directly attack the side chains of arginine, proline, threonine, and lysine residues (Shannon and Weerapana, 2015). OH radicals also attack the target proteins by α-amination pathway. The cysteine, lysine, or histidines are attacked by carbonyls through reacting with reactive aldehydes such as malondialdehyde (Camejo et al., 2015). Carbonylation is also reported in chloroplasts of Arabidopsis during high light condition (Madian and Regnier, 2010). The chloroplastic proteins, such as cysteine synthase, Asp kinase, and Rubisco, undergo carbonylation, which results in their

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altered functions (Madian and Regnier, 2010). In Arabidopsis and soybean, there was a marked increase in protein carbonyl due to exposure of plants to elevated levels of CO2 (Crofts, 2004). In addition, several mitochondrial enzymes, such as aconitase, pyruvate dehydrogenase, and glycine decarboxylases, are also altered due to carbonylation that affects normal metabolism. Carbonylated proteins are identified, and their analyses have revealed their signaling functions (Smakowska et al., 2016). 20.3.3.5 Nitrosylation ROS as well as RNS are responsible for inducing abiotic stress in the plants (Camejo et al., 2013). When present in higher levels, these RNS and ROS disturb the normal balance maintaining the cellular redox homeostasis (Mittler, 2017). Increased RNS induces nitrooxidative stress, which leads to damage to the plants (Camejo et al., 2013). On the other hand, nitric oxide (NO) plays a role in inter and intracellular signaling and an important role in cellular functions (Bonomini et al., 2015). It regulates different proteins and enzymes by altering their structure by S-nitrosylation. Nitrosylation is a process in which NO binds with the thiol group of cysteine by covalent binding and thus regulates the function of proteins. Interaction of NO with sulfhydryl groups and transition metals alters the proteins structure and function, and S-nitrothiols and metal nitrosyls are found as products (Bonomini et al., 2015). Salinity stress induces nitrosylation in enzymes involved in respiration, antioxidation, and photorespiration to keep homeostasis under stress conditions (Baena et al., 2017). Forty-nine proteins are reported to be S-nitrosylated on exposure to salt stress in Citrus aurantium leaves (Tanou et al., 2009). Further, salt stress and low temperature
induced modification due to S-nitrosylation was studied in Arabidopsis and rice, respectively (Chaki et al., 2015; Mun et al., 2018). Maintaining of NO/ROS balance inside the cell to regulate the redox state will be a future challenge. Many scientists have reported the protective role of NO during stressful conditions such as heavy metals, salinity, UV radiations, and drought (Camejo et al., 2013; Fancy et al., 2017; Simontacchi et al., 2015). Further, different species have been identified with altered NO production on exposure to environmental stress (Farnese et al., 2016; Savvides et al., 2016; Oz et al., 2015). Moreover, transgenic plants with elevated NO production have been studied by many researchers (Fares et al., 2011).

20.4 Regulation of protein stability Plants cope with the sudden and abrupt changes in the environment by evolving an efficient protein repair system and general protein stability mechanism. The proteins are the biological macromolecules without which no metabolic and physiological processes can be carried out (Mittler, 2017). Proteins maintain a unique and three-dimensional structure by folding its polypeptide chains. Stress induces alteration in the protein folding, which results in the change of native conformation and hence affects the stability (Gavrilov et al., 2015). Protein misfolding gives rise to degradation of the protein and affects associated functions. The damaged or misfolded proteins accumulated on exposure to stressful conditions are removed by ubiquitin protease system or UPS (Miller et al., 2015). The UPS not only modulates the level of regulatory proteins but also facilitates plants in carrying out different pathways related to the plant’s stress tolerance (Miller et al., 2015). Another most extensively

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studied sensing protein includes Ca21 sensing protein or CaM, which is involved in transduction of Ca21 signals and influences a number of CaM-binding proteins (Clister et al., 2015). Many researchers have reported the key role of CaM in ion uptake, generation of ROS, and regulation of various transcription factors such as CAMTA3, WRKY39, and GTL1 (Virdi et al., 2015). Different kinase and phosphatase activities are reported to be regulated by CaM. Moreover, contemporary studies have proved that it has a well-defined role in maintaining homeostasis among several vital processes inside the cell in plants. Identification of different CaM-binding proteins can prove to be useful in gathering a deep insight of molecular mechanisms involved in abiotic stress tolerance.

20.4.1 Hormone-mediated stress tolerance in plants Plants can regulate stress tolerance and control the growth by altering the levels of production, distribution, and finally the signal transduction of different hormones and promotes survival in the stressful condition. 20.4.1.1 Auxin Auxin is the not only the primary growth regulator for growth of plant and development but also plays a very important role in providing tolerance to different environmental stress in plants (Wani et al., 2016). Intensive investigations in the field of genomics and expression analysis have revealed its expression in abiotic stress conditions. Its expression was studied during drought, salinity, and ABA exposure on plants. In order to survive in stressful environments, a plant adapts by redirecting its growth, limiting the damages, and facilitating repair of the damages (Vinocur et al., 2017). Auxin-mediated responses are also reported in many plant species during stressful conditions (Ding et al., 2015). Dai et al. (2013) have reported decreased synthesis of auxin on disturbing the functional YUCCA pathway in A. thaliana. Suppression of expression of YUC2 and YUC6 genes can decline the synthesis of auxin in developing anthers, which results in male sterility, hence decreasing yield (Kim et al., 2013). Moreover, overexpressing of YUC2 and YUC6 genes elevated the synthesis of auxin and hence improved drought (Kim et al., 2013). Further studies revealed that increased levels of auxins regulate different abiotic stress
associated genes such as RAB18, RD22, RD29A, DREB2A, and DREB2B (Shi et al., 2015). WRKY23 gene, which is a member of WRKY family and induced by auxin, is associated with abiotic stress (Dai et al., 2013). Auxin induces increased shoot branching and altered shape, which protects from salt and drought stress in transgenic plants in comparison to the wild types (Dai et al., 2013). 20.4.1.2 Brassinosteroids Brassinosteroids are considered as novel steroidal phytohormones, which are ubiquitous in plant kingdom. It is linked to the abiotic stress tolerance in plants as it is associated with a number of biochemical as well as physiological processes (Wani et al., 2016). It plays various important roles in the activation and progression of cellular proliferation, vascular differentiation, male fertility, leaf development, and senescence (Vardhini, 2012). Moreover, it also takes part in the regulation of different genes affecting morphogenesis. It

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induces RBOH transcription and increased NADPH oxidase activity, accumulation of H2O2, and induction of ABA biosynthesis (Gill and Tuteja 2010). The potential of brassinosteroids in improving growth and yield under stressful conditions, such as high temperature, cold, drought, salinity, and excessive heavy metals, has also been studied (C ¸ oban and Baydar, 2016; You and Chan, 2015; Ryu and Cho, 2015). The mutant plants, which were brassinosteroid-deficient, showed dwarf and etiolated morphological features, which proved the importance of brassinosteroids in growth and development (Rao et al., 2002). Brassinosteroids also interact with other plant hormones, such as cytokinins, auxins, ABA, gibberellins, salicylic acid, ethylene, and jasmonic acid, to regulate different metabolic pathways (Domagalska et al., 2010; Manzano et al., 2011; Divi et al., 2010; Krishna et al., 2017). Three different brassinosteroids, such as 28-homobrassinolide (28-homoBL), brassinolide (BL), and 24-epiBL, were used for experimental studies (Vardhini et al., 2006). Amelioration of cadmium toxicity
induced damaging effects was reported in tomato and Raphanus sativa using 28-homoBL and 24-epiBL, respectively (Bajguz, 2009). These experiments showed brassinosteroid-mediated improvement in photosynthetic machinery, enhanced antioxidant system, and improved yield. 20.4.1.3 Gibberellins The role of gibberellins in tolerance to cold, salt, and osmotic stress is increasingly studied. Increased gibberellic acid (GA) synthesis contributes to enhanced growth of the plant and helps in surviving under stress (Sponsel and Hedden, 2004). Gibberellin controls cell division and cell elongation process by regulating the DELLA proteins (Hirano et al., 2012). Increased DELLA activity results in ROS-quenching capacity and improved survival. In A. thaliana, exposure of salinity caused a decrease of the bioactive Gas, which in turn induced DELLA protein accumulation (Feng et al., 2008). Moreover, salt stress quadrupled DELLA proteins and inhibited growth of roots and shoots while the flowering time was delayed (Achard et al., 2006). Many studies have shown that DELLA proteins take part in providing protection against freezing-induced stress (Achard et al., 2008). In salinity as well as freezing-stress tolerance, dehydration responsive element binding protein (DREB1)/CBF family transcription factors are reported to play a role in reducing the level of bioactive GA (Magome et al., 2008). GA is also reported to take part in providing tolerance in response to flooding. GA allows shoot to grow out of the water level at the surface by mediating internode elongation (Hattori et al., 2009). Further, an important role of GA is to provide tolerance to mild osmotic stress in A. thaliana as it restrains the accumulation of ROS (Fukao et al., 2006). Increased GA biosynthesis is also reported to confer tolerance on shading and submergence in plants. Signaling pathway associated with jasmonic acid is also another pathway by which GA modulates stress tolerance in plants. 20.4.1.4 Abscisic acid The stress harmone Abscissic acid (ABA) plays a significant role in controlling various stress signalling and associated downstream processes in plants (Mehrotra et al., 2014). Water deficit and high salinity stress induces the synthesis of ABA and its accumulation, which results in closing of stomata and maintenance of water balance (Ng et al., 2014). Stress is induced by two signaling pathways: one is ABA-dependent and the other is ABA-independent. Expression of ABA takes place through ABA-responsive element, that

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is, a cis-acting element. Some transcription factors belonging to protein MYC, MYB, and NAC families function in an ABA-dependent manner (Verma et al., 2016). The DREBINDING PROTEIN (DREB) transcription factors are also regulated by ABA-dependent pathways under osmotic stress (Upadhyay et al., 2017). Synthesis of many ABA biosynthesis genes, such as 9-cis-epoxycarotenoid dioxygenase (NCED), molybdenum cofactor sulfurase (MCSU), ABA-aldehyde oxidase (AAO), and zeaxanthin oxidase (ZEP), are reported to be induced by calcium-dependent phosphorylation pathway (Vishwakarma et al., 2017). In a study, overexpression of AtMYC2 and AtMYB2 transcription factors improved osmotic tolerance in A. thaliana, which again confirms its significant role in abiotic stress response (Verma et al., 2016). Thus it is evident that ABA regulates tolerance mechanism in abiotic stress in plants. Increased levels of ABA were observed in maize, rice, sorghum, barley, soybean, and wheat on exposure to drought stress, while some earlier researchers have reported enhanced ABA accumulation in cold and salt stress in many plant species (He et al., 2018; Cai et al., 2015; Mittal et al., 2017; Vishwakarma et al., 2017; Li et al., 2016; Tripathi et al., 2016). As far as exogenous application of ABA is concerned, ABA enhances drought tolerance and salinity in many crops (Waterland et al., 2010). It induces synthesis of osmoprotectant enzymes by inducing the expression of many genes regulating the opening and closing of stomatal aperture (Du et al., 2013).

20.4.2 Ubiquitin protease system Ubiquitin, which is a universally expressed, stable, and highly conserved eukaryotic protein, plays a major role in posttranslational modification and regulatory functions. It recently appeared as a crucial factor in plant abiotic stress as it has a well-defined role in selective proteolysis by ubiquitin
proteasome system (UPS) (Pokhilko et al., 2011). In A. thaliana over 6% of the coding genes are reported to belong to 26S UPS. The UPS regulates embryogenesis, photomorphogenesis, and organ development and provides adaptation to various stresses including salinity, temperature extremities, and nutrient deprivation (Sharma et al., 2015). Protein ubiquitination occurs via the covalent binding of ubiquitin with lysine residue of the protein. E3 ubiquitin ligase maintains the salinity and drought stress by ABA signaling (Rao et al., 2018). Some E3 ligases are the “Keep on Going” or KEG ligases (Liu and Stone 2010; Lee et al., 2010), the “ABA-hypersensitive DCAF1” or ABD1 (Seo et al., 2014), the two CUL4
DDB1 E3 ligases DWD hypersensitive 1 and 2 (Lee et al., 2010), and dehydration responsive element binding protein or DREB 2A. The RINGtype E3 ligases are DREB2A-interacting protein or DRI or 1 and DRIP2 (Guerra et al., 2015). The RING-type E3 ligases, such as Arabidopsis toxicos EN Levadura (ATL) 6 and ATL31, control the availability of a 14-3-3 protein needed for seedling response against carbon/nitrogen stress (Ali et al., 2019). The carbon and nitrogen ratio needs to be maintained, as it regulated the germination and seed establishment. Oryza sativa droughtinduced SINA protein 1 (OsDIS1) is a RING-type E3, which has high resemblance in sequences with Arabidopsis SINAT5 (McNeilly et al., 2018). Lack of functional OsDIS1 increases tolerance to drought in rice, while transgenic rice plants, having overexpressed OsDIS1, showed reduced tolerance to drought.

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20.4.3 Calmodulin-mediated alterations The Ca21 signals take part in many key developmental and adaptive processes at the initiation of any physiological stimuli. CaM and CaM-like proteins are both called primary Ca21 sensors that regulate various target proteins (Ranty et al., 2016). These proteins generate Ca21 signals that initiate Ca21-associated regulation and expression of genes. CaM interacts with Ca21 and undergoes conformational changes and influences the activities of CaM-binding proteins (Gonza´lez-Fontes et al., 2017). These CaM-binding proteins are involved in a key role in stress-tolerance mechanism in plants. It also regulates the metal ion uptake, production of ROS, and modulation of different transcription factors such as GTL1, WRKY39, and CAMTA3 (Park et al., 2010). Researchers have identified the following ways of Ca21 regulation in plants: A. Binding of Ca21 directly to transcriptional factors and alteration of its activity (Zhu, 2016). B. Ca21/CaM complex binds with promoter sequences such as a transcription factor and affects the gene expression (Zeng et al., 2015). C. Direct interaction of Ca21/CaM complex and transcription factors along with the regulation of their transcriptional activities (Takemoto-Kimura et al., 2017). D. Indirect interaction of Ca21/CaM complex with transcription factor
binding protein is a multicomponent transcriptional machinery by which it can alter their function (Zeng et al., 2015). E. Ca21/CaM complex alters the phosphorylation process of transcription factors and hence influences the gene expression. This process takes place via CaM-binding protein kinase and a CaM-binding protein phosphatase (Evans et al., 2018). Further, Ca21 and CaM also control different transcriptional regulation
associated mechanisms, which are also studied.

20.5 Overexpression of organelle proteins in transgenic plants improves stress tolerance Different abiotic factors, which include salt, drought, and heavy-metal stress, are the key limiting factors that affect growth and development of crops. Plants are able to cope with the situation by adapting different mechanisms, which lead to alterations in protein expression and hence the morphological features (Hasanuzzaman et al., 2013). Understanding the key regulatory mechanisms in these plants species is the initiating step for developing tolerant crops (Zandalinas et al., 2018; Pandey et al., 2019). Proteomics has developed many tools, which help in evaluating the regulation of proteins and subcellular proteins including transporters of water and ions, transcriptional regulators, and ROS scavengers under stressful conditions (Janmohammadi et al., 2015; Pandey et al., 2019). Overexpression of stress-responsive genes is one of the major approaches in the production of tolerant crops (Pandey et al., 2019). Many scientists have reported overexpression of subcellular proteins in nucleus, plasma membrane, vacuole, ER, chloroplast, and mitochondria in which the nucleus contains 42% of the overexpressed proteins, while the chloroplast, plasma membrane, and ER localizes 23%, 13%, and 10% of the overexpressed proteins (Nouri and

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Komatsu, 2013). The plasma membrane is involved in perception of the signals, cellular homeostasis, and expression of several plasma membrane proteins that help in tolerating chilling stress in plants (Kumar et al., 2018). Phospholipase Dδ is a plasma membrane associated protein that produces phosphatidic acid by hydrolyzing the membrane phospholipids, has been reported to be over expressed during cold acclimation (Margutti et al., 2017). Salicornia brachiata is a well-known halophyte that grows in salt marshes, which is being studied to develop an understanding toward the regulation of salt and droughtresponsive genes (Singh et al., 2016). Transgenic tobacco plants that constitutively overexpressed SbSRP gene showed improved salinity and osmotic stress tolerance (Udawat et al., 2016). To increase the protein content in rice, increased lysine and threonine-encoded genes were introduced into rice genome, and transgenic varieties were developed (Jiang et al., 2016). Moreover, quality protein maize was developed containing doubled lysine content in seeds (Babu et al., 2015). Similar experiments were also carried out in Arabidopsis, canola, soybean, and tobacco for improving lysine, threonine, and methionine content (Liu et al., 2015; Chang et al., 2015; Cohen et al., 2017). Research is still continued to develop transgenic varieties in order to improve tolerance inside the plant system.

20.6 Synthesis of the novel proteins Plants being sessile face diverse biotic and abiotic stresses, which affect its growth and productivity. Plants have evolved a complex response mechanism that protects them from the harmful effect of stress (Ohama et al., 2017). Among several options, synthesis of novel regulatory proteins is an important mechanism of the stress-tolerance mechanism inside the plant system (Zhang et al., 2015). Stress-responsive signaling pathways depend upon the nature and type of stress to which the plant is exposed. It is now possible to identify the novel regulatory proteins and their function in abiotic stress tolerance. Progress in proteomics approaches include 2D gel electrophoresis, LC
MS/MS, which are being used for numerous studies addressing rice response to major environmental stresses (Agrawal et al., 2016). Computational and experimental approaches are used to get a particular conformation of protein by uniquely folding it (Lin et al., 2016). The solid-phase peptide synthesis and solution synthesis methods are applied for inducing modification and designing of proteins (Robertson et al., 2016). Foundation of catalytic sites is the major challenge in the construction of the protein. Different studies were carried out in order to develop four α-helix bundle proteins exhibiting structural similarity with that of native proteins (Boyken et al., 2016). Designing metal-binding sites needs exact positioning of amino acid residues within the protein. As far as the designing and synthesis of enzymes are concerned, catalytic sites are created in designed proteins (Heinisch et al., 2015). As an example, Pyrococcus furiosus has been synthesized, which is the modified version of desulfovibrio gigas ferredoxin II, and spectrophotometrically and electrochemically proved to have similar properties (Liu et al., 2015). The various data illustrate incorporation of the biological cofactors in modified version of native proteins or designed proteins to regulate its function. In addition, a deeper understanding is being developed regarding packing defects and dynamic properties of mutated protein (Zhao et al., 2015). This knowledge will be helpful in developing stress tolerance in crops by modifying stress-susceptible proteins.

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20.7 Conclusion and future aspects It has been the matter of great concern all over the globe to cope with abiotic stresses, such as drought, temperature extremities including heat and cold, water logging, salinity, and heavy-metal toxicity, which affect crop yield. Abiotic stresses cause modification in the protein conformation and induce alteration in the genes involved in signaling cascades, transcriptional regulation, uptake, and transport of water and ion. Plant responses to numerous abiotic stresses by posttranslational modifications, such as phosphorylation, glycosylation, acetylation, and succinylation, have been summarized. Moreover, posttranslational alterations of histone and tubulins, which play a fundamental role in most of the biological processes, are also highlighted. ROS, which are significantly accumulated during abiotic stress, eventually leads to protein oxidative modifications by different processes such as sulfonylation, glutathionylation, tryptophan oxidation, carbonylation, and nitrosylation. Recent research findings elaborate critical roles of phytohormones, such as gibberellins, brassinosteroids, auxins, and ABA, in signaling networks responsible for conferring an efficient defense response. Selective proteolysis by UPS and CaM-associated alterations has emerged as a major factor in plant response and adaptation with the environmental stresses. Recent approaches regarding overexpression of proteins in generating transgenic plants having enhanced tolerance capabilities against abiotic stresses are also reviewed. Diverse experimental and computational approaches regarding protein designing and synthesis of novel proteins is an exciting step for developing stress-tolerant plants. Much work has been carried to identify the role of different proteins in combating the stress; however, regulation of proteins varies among different species, which still needs to be studied. Furthermore, complete characterization of all the proteins accumulating at the time of different abiotic stresses still remains unachieved. Alteration in protein conformation and protein stability are reported by many researchers, but rules of protein folding are still a matter of research. Detailed investigation regarding the regulation of UPS and CaM-associated protein alterations will broaden our knowledge and help develop transgenic plants by engineering these proteins. Despite that, different proteins have been overexpressed to develop tolerant varieties, but the transgenic varieties are the model plants and not useful crop varieties.

References Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., et al., 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91
94. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., Genschik, P., 2008. The cold-inducible CBF1 factordependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20, 2117
2129. Aghaei, K., Ehsanpour, A.A., Komatsu, S., 2009. Potato responds to salt stress by increased activity of antioxidant enzymes. J. Integr. Plant Biol. 51, 1095
1103. Agrawal, L., Gupta, S., Mishra, S.K., Pandey, G., Kumar, S., Chauhan, P.S., et al., 2016. Elucidation of complex nature of PEG induced drought-stress response in rice root using comparative proteomics approach. Front. Plant Sci. 7, 1466. Ahmed, F., Rafii, M.Y., Ismail, M.R., Juraimi, A.S., Rahim, H.A., Asfaliza, R., Latif, M.A., 2012. Waterlogging tolerance of crops: breeding, mechanism of tolerance, molecular approaches, and future prospects. BioMed Res. Int. 2013.

Plant Life under Changing Environment

532

20. Proteomics in relation to abiotic stress tolerance in plants

Ahsan, N., Lee, D.G., Kim, K.H., Alam, I., Lee, S.H., Lee, K.-W., et al., 2010. Analysis of arsenic stress-induced differentially expressed proteins in rice leaves by two-dimensional gel electrophoresis coupled with mass spectrometry. Chemosphere 78, 224
231. Aiese Cigliano, R., Sanseverino, W., Cremona, G., Ercolano, M.R., Conicella, C., Consiglio, F.M., 2013. Genomewide analysis of histone modifiers in tomato: gaining an insight into their developmental roles. BMC Genomics 14, 57. Al Hassan, M., 2018. Comparative Analyses of Plant Responses to Drought and Salt Stress in Related Taxa: A Useful Approach to Study Stress Tolerance Mechanisms (Doctoral dissertation). Ali, M.R., Uemura, T., Ramadan, A., Adachi, K., Nemoto, K., Nozawa, A., et al., 2019. The Ring-type E3 ubiquitin ligase JUL1 targets the VQ-motif protein JAV1 to coordinate jasmonate signaling. Plant Physiol. 179 (4), 1273
1284. ´ ., Serna, A., Gotor, C., Romero, L.C., 2015. S-sulfhydration: a cysteine posttranslational modification in Aroca, A plant systems. Plant Physiol. 168 (1), 334
342. Ashraf, M., 2014. Stress-induced changes in wheat grain composition and quality. Crit. Rev. Food Sci. Nutr. 54, 1576
1583. Available from: https://doi.org/10.1080/10408398.2011.644354. Astegno, A., Bonza, M.C., Vallone, R., La Verde, V., D’Onofrio, M., Luoni, L., et al., 2017. Arabidopsis calmodulin-like protein CML36 is a calcium (Ca21) sensor that interacts with the plasma membrane Ca21ATPase isoform ACA8 and stimulates its activity. J. Biol. Chem. 292 (36), 15049
15061. Babu, B.K., Agrawal, P.K., Saha, S., Gupta, H.S., 2015. Mapping QTLs for opaque2 modifiers influencing the tryptophan content in quality protein maize using genomic and candidate gene-based SSRs of lysine and tryptophan metabolic pathway. Plant Cell Rep. 34 (1), 37
45. Baena, G., Feria, A.B., Echevarrı´a, C., Monreal, J.A., Garcı´a-Maurin˜o, S., 2017. Salinity promotes opposite patterns of carbonylation and nitrosylation of C4 phosphoenolpyruvate carboxylase in sorghum leaves. Planta 246 (6), 1203
1214. Baeza, J., Smallegan, M.J., Denu, J.M., 2016. Mechanisms and dynamics of protein acetylation in mitochondria. Trends Biochem. Sci. 41 (3), 231
244. Bajguz, A., 2009. Brassinosteroid enhanced the level of abscisic acid in Chlorella vulgaris subjected to short-term heat stress. J. Plant Physiol. 166, 882
886. Baker, M.R., Tabb, D.L., Ching, T., Zimmerman, L.J., Sakharov, I.Y., Li, Q.X., 2016. Site-specific N-glycosylation characterization of windmill palm tree peroxidase using novel tools for analysis of plant glycopeptide mass spectrometry data. J. Proteome Res. 15, 2026
2038. Ban, Y., Kobayashi, Y., Hara, T., Hamada, T., Hashimoto, T., Takeda, S., et al., 2013. Tubulin is rapidly phosphorylated in response to hyperosmotic stress in rice and Arabidopsis. Plant Cell Physiol. 2013 (54), 848
858. Banerjee, A., Roychoudhury, A., 2015. WRKY proteins: signaling and regulation of expression during abiotic stress responses. Sci. World J. 2015. Banerjee, A., Roychoudhury, A., 2016. Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul. 79 (1), 1
17. Bonomini, F., Rodella, L.F., Rezzani, R., 2015. Metabolic syndrome, aging and involvement of oxidative stress. Aging Dis. 6 (2), 109. Boudet, J., Buitink, J., Hoekstra, F.A., Rogniaux, H., Larre´, C., Satour, P., et al., 2006. Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol. 140, 1418
1436. Boursiac, Y., Leran, S., Corratge-Faillie, C., Gojon, A., Krouk, G., Lacombe, B., 2013. ABA transport and transporters. Trends Plant Sci. 18, 325
333. Boyken, S.E., Chen, Z., Groves, B., Langan, R.A., Oberdorfer, G., Ford, A., et al., 2016. De novo design of protein homo-oligomers with modular hydrogen-bond network
mediated specificity. Science 352 (6286), 680
687. Budak, H., Hussain, B., Khan, Z., Ozturk, N.Z., Ullah, N., 2015. From genetics to functional genomics: improvement in drought signaling and tolerance in wheat. Front. Plant Sci. 6, 1012. Byrt, C.S., Platten, J.D., Spielmeyer, W., 2007. HKT1;5-like cation transporters linked to Na1 exclusion loci in wheat, Nax2 and Kna1. Plant Physiol. 143 (4), 1918
1928. Cai, S., Jiang, G., Ye, N., Chu, Z., Xu, X., Zhang, J., et al., 2015. A key ABA catabolic gene, OsABA8ox3, is involved in drought stress resistance in rice. PLoS One 10 (2), p. e0116646. Camejo, D., Romero-Puertas, M.D.C., Rodriguez-Serrano, M., Sandalio, L.M., Lazaro, J.J., Jimenez, A., et al., 2013. Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J. Proteomics 79, 87
99.

Plant Life under Changing Environment

References

533

Camejo, D., Jimenez, A., Palma, J.M., Sevilla, F., 2015. Proteomic identification of mitochondrial carbonylated proteins in two maturation stages of pepper fruits. Proteomics 15, 2634
2642. Catala´, C., Howe, K.J., Hucko, S., Rose, J.K., Thannhauser, T.W., 2011. Towards characterization of the glycoproteome of tomato (Solanum lycopersicum) fruit using Concanavalin A lectin affinity chromatography and LC-MALDI-MS/MS analysis. Proteomics 11, 1530
1544. Chaki, M., Shekariesfahlan, A., Ageeva, A., Mengel, A., von Toerne, C., Durner, J., et al., 2015. Identification of nuclear target proteins for S-nitrosylation in pathogen-treated Arabidopsis thaliana cell cultures. Plant Sci. 238, 115
126. Chang, Y., Shen, E., Wen, L., Yu, J., Zhu, D., Zhao, Q., 2015. Seed-specific expression of the Arabidopsis AtMAP18 gene increases both lysine and total protein content in maize. PLoS One 10 (11), e0142952. Chao, Q., Gao, Z.F., Wang, Y.F., Li, Z., Huang, X.H., Wang, Y.C., et al., 2016. The proteome and phosphoproteome of maize pollen uncovers fertility candidate proteins. Plant Mol. Biol. 91, 287
304. Chen, J., Gao, L., Baek, D., Liu, C., Ruan, Y., Shi, H., 2015. Detoxification function of the Arabidopsis sulphotransferase AtSOT 12 by sulphonation of xenobiotics. Plant Cell Environ. 38 (8), 1673
1682. Choudhury, F.K., Rivero, R.M., Blumwald, E., Mittler, R., 2017. Reactive oxygen species, abiotic stress and stress combination. Plant J. 90 (5), 856
867. Clister, T., Mehta, S., Zhang, J., 2015. Single-cell analysis of G-protein signal transduction. J. Biol. Chem. 290 (11), 6681
6688. ¨ ., Baydar, N.G., 2016. Brassinosteroid effects on some physical and biochemical properties and secondary C ¸ oban, O metabolite accumulation in peppermint (Mentha piperita L.) under salt stress. Ind. Crops Prod. 86, 251
258. Cohen, H., Hacham, Y., Matityahu, I., Amir, R., 2017. Elucidating the effects of higher expression level of cystathionine γ-synthase on methionine contents in transgenic Arabidopsis, soybean and tobacco seeds. Sulfur Metabolism in Higher Plants-Fundamental, Environmental and Agricultural Aspects. Springer, Cham. Colebrook, E.H., Thomas, S.G., Phillips, A.L., Hedden, P., 2014. The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol. 217, 67
75. Cosgrove, D.J., 2015. Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J. Exp. Bot. 67 (2), 463
476. Crofts, A.R., 2004. The cytochrome bc1 complex: function in the context of structure. Annu. Rev. Physiol. 66, 689
733. Csisza´r, J., Brunner, S., Horva´th, E., Bela, K., Ko¨dmo¨n, P., Riyazuddin, R., et al., 2018. Exogenously applied salicylic acid maintains redox homeostasis in salt-stressed Arabidopsis f20-01-9780128182048 mutants expressing cytosolic roGFP1. Plant Growth Regul. 86, 181
194. Dai, X., Mashiguchi, K., Chen, Q., Kasahara, H., Kamiya, Y., Ojha, S., et al., 2013. The biochemical mechanism of auxin biosynthesis by an Arabidopsis YUCCA flavin-containing monooxygenase. J. Biol. Chem. 288, 1448
1457. de Zelicourt, A., Colcombet, J., Hirt, H., 2016. The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci. 21 (8), 677
685. Ding, Z.J., Yan, J.Y., Li, C.X., Li, G.X., Wu, Y.R., Zheng, S.J., 2015. Transcription factor WRKY 46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis. Plant J. 84 (1), 56
69. Divi, U.K., Rahman, T., Krishna, P., 2010. Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol. 10 (1), 151. Domagalska, M.A., Sarnowska, E., Nagy, F., Davis, S.J., 2010. Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PLoS One 5, e14012. Du, Y.L., Wang, Z.Y., Fan, J.W., Turner, N.C., He, J., Wang, T., et al., 2013. Exogenous abscisic acid reduces water loss and improves antioxidant defence, desiccation tolerance and transpiration efficiency in two spring wheat cultivars subjected to a soil water deficit. Funct. Plant Biol. 40, 494
506. Duan, J., Zhang, M., Zhang, H., Xiong, H., Liu, P., Ali, J., et al., 2012. OsMIOX, a myo-inositol oxygenase gene, improves drought tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). Plant Sci. 196, 143
151. Durcan, T.M., Fon, E.A., 2015. The three P’s of mitophagy: PARKIN, PINK1, and post-translational modifications. Genes Dev. 29 (10), 989
999. Ehrenshaft, M., Deterding, L.J., Mason, R.P., 2015. Tripping up Trp: Modification of protein tryptophan residues by reactive oxygen species, modes of detection, and biological consequences. Free Radical Biol. Med. 89, 220
228.

Plant Life under Changing Environment

534

20. Proteomics in relation to abiotic stress tolerance in plants

Emon, J.M.V., 2016. The omics revolution in agricultural research. J. Agric. Food Chem. 64, 36
44. Available from: https://doi.org/10.1021/acs.jafc.5b04515. Espinosa-Diez, C., Miguel, V., Mennerich, D., Kietzmann, T., Sa´nchez-Pe´rez, P., Cadenas, S., et al., 2015. Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol. 6, 183
197. Evans, P.R., Gerber, K.J., Dammer, E.B., Duong, D.M., Goswami, D., Lustberg, D.J., et al., 2018. Interactome analysis reveals regulator of G protein signaling 14 (RGS14) is a novel calcium/calmodulin (Ca21/CaM) and CaM kinase II (CaMKII) binding partner. J. Proteome Res. 17 (4), 1700
1711. Fancy, N.N., Bahlmann, A.K., Loake, G.J., 2017. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 40 (4), 462
472. Fares, A., Rossignol, M., Peltier, J.B., 2011. Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem. Biophys. Res. Commun. 416, 331
336. Farnese, F.S., Menezes-Silva, P.E., Gusman, G.S., Oliveira, J.A., 2016. When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Front. Plant Sci. 7, 471. Feng, S., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J., Wang, F., et al., 2008. Coordinated regulation of Arabidopsisthaliana development by light and gigibberellins. Nature 451 (7177), 475. Forni, C., Duca, D., Glick, B.R., 2017. Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil 410 (1-2), 335
356. Fox, A.R., Maistriaux, L.C., Chaumont, F., 2017. Toward understanding of the high number of plant aquaporin isoforms and multiple regulation mechanisms. Plant Sci. 264, 179
187. Friso, G., van Wijk, K.J., 2015. Post translational protein modifications in plant metabolism. Plant Physiol. 169 (3), 1469
1487. Fu, C., Liu, X.X., Yang, W.W., Zhao, C.M., Liu, J., 2016. Enhanced salt tolerance in tomato plants constitutively expressing heat-shock protein in the endoplasmic reticulum. Genet. Mol. Res 15. Fukao, T., Xu, K., Ronald, P.C., Bailey-Serres, J., 2006. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18, 2021
2034. Gao, Y., Dai, X., Zheng, Z., Kasahara, H., Kamiya, Y., Chory, J., et al., 2016. Overexpression of the bacterial tryptophan oxidase RebO affects auxin biosynthesis and Arabidopsis development. Sci. Bull. 61 (11), 859
867. Gavrilov, Y., Shental-Bechor, D., Greenblatt, H.M., Levy, Y., 2015. Glycosylation may reduce protein thermodynamic stability by inducing a conformational distortion. J. Phys. Chem. Lett. 6 (18), 3572
3577. Gill, S.S., Tuteja, N., 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909
930. Gong, F., Hu, X., Wang, W., 2015. Proteomic analysis of crop plants under abiotic stress conditions: where to focus our research? Front. Plant Sci. 6, 418. Available from: https://doi.org/10.3389/fpls.2015.00418. Gonza´lez-Fontes, A., Navarro-Gochicoa, M.T., Ceacero, C.J., Herrera-Rodrı´guez, M.B., Camacho-Cristo´bal, J.J., Rexach, J., 2017. Understanding calcium transport and signaling, and its use efficiency in vascular plants. Plant Macronutrient Use Efficiency. Academic Press, pp. 165
180. Gray, H.B., Winkler, J.R., 2015. Hole hopping through tyrosine/tryptophan chains protects proteins from oxidative damage. Proc. Natl. Acad. Sci. U. S. A. 112 (35), 10920
10925. Guerra, D., Crosatti, C., Khoshro, H.H., Mastrangelo, A.M., Mica, E., Mazzucotelli, E., 2015. Post-transcriptional and post-translational regulations of drought and heat response in plants: a spider’s web of mechanisms. Front. Plant Sci. 6, 57. Guo, Q., Zhang, J., Gao, Q., Xing, S., Li, F., Wang, W., 2008. Drought tolerance through overexpression of monoubiquitin in transgenic tobacco. J. Plant Physiol. 165, 1745
1755. Gustavsson, N., Kokke, B.P., Harndahl, U., Silow, M., Bechtold, U., Poghosyan, Z., et al., 2002. A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein. Plant J. 29, 545
553. ´ Gzyl, J., Chmielowska-Ba˛k, J., Przymusinski, R., Gwo´z´ d´z, E.A., 2015. Cadmium affects microtubule organization and post-translational modifications of tubulin in seedlings of soybean (Glycine max L.). Front. Plant Sci. 6, 937. Hara, M., Furukawa, J., Sato, A., Mizoguchi, T., Miura, K., 2012. Abiotic stress and role of salicylic acid in plants. In: Parvaiza, A., Prasad, M.N.V. (Eds.), Abiotic Stress Responses in Plants. Springer, New York, pp. 235
251.

Plant Life under Changing Environment

References

535

Harmoko, R., Yoo, J.Y., Ko, K.S., Ramasamy, N.K., Hwang, B.Y., Lee, E.J., et al., 2016. N-glycan containing a core α1, 3-fucose residue is required for basipetal auxin transport and gravitropic response in rice (Oryza sativa). New Phytol. 212, 108
122. Hasanuzzaman, M., Nahar, K., Fujita, M., 2013. Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmed, P., Azooz, M.M., Prasad, M.N.V. (Eds.), Ecophysiology and Responses of Plants under Salt Stress. Springer, New York, pp. 25
87. Hattori, Y., Nagai, K., Furukawa, S., Song, X.-J., Kawano, R., Sakakibara, H., et al., 2009. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460, 1026
1030. He, H., He, L., Gu, M., 2015. Signal transduction during aluminum-induced secretion of organic acids in plants. Biol. Plantarum 59 (4), 601
608. He, D., Wang, Q., Li, M., Damaris, R.N., Yi, X., Cheng, Z., et al., 2016. Global proteome analyses of lysine acetylation and succinylation reveal the widespread involvement of both modification in metabolism in the embryo of germinating rice seed. J. Proteome Res. 15, 879
890. He, Z., Zhong, J., Sun, X., Wang, B., Terzaghi, W., Dai, M., 2018. The maize ABA receptors ZmPYL8, 9, and 12 facilitate plant drought resistance. Front. Plant Sci. 9, 422. Heinisch, T., Pellizzoni, M., Du¨rrenberger, M., Tinberg, C.E., Ko¨hler, V., Klehr, J., et al., 2015. Improving the catalytic performance of an artificial metalloenzyme by computational design. J. Am. Chem. Soc. 137 (32), 10414
10419. Hirano, K., Kouketu, E., Katoh, H., Aya, K., Ueguchi-Tanaka, M., Matsuoka, M., 2012. The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity. Plant J. 71, 443
453. Hong, Y., Yuan, S., Sun, L., Wang, X., Hong, Y., 2018. Cytidinediphosphate-diacylglycerol synthase 5 is required for phospholipid homeostasis and is negatively involved in hyperosmotic stress tolerance. Plant J. 94, 1038
1050. Hou, H., Wang, P., Zhang, H., Wen, H., Gao, F., Ma, N., et al., 2015. Histone acetylation is involved in gibberellinregulated sodCp gene expression in maize aleurone layers. Plant Cell Physiol. 56, 2139
2149. Huang, R.F., Lloyd, C.W., 1999. Gibberellic acid stabilises microtubules in maize suspension cells to cold and stimulates acetylation of α-tubulin. FEBS Lett. 443, 317
320. Huang, S., Spielmeyer, W., Lagudah, E.S., 2006. A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol. 142 (4), 1718
1727. Hwang, I., Sheen, J., Mu¨ller, B., 2012. Cytokinin signaling networks. Annu. Rev. Plant Biol. 63, 353
380. Janmohammadi, M., Zolla, L., Rinalducci, S., 2015. Low temperature tolerance in plants: changes at the protein level. Phytochemistry 117, 76
89. Jiang, S.Y., Ma, A., Xie, L., Ramachandran, S., 2016. Improving protein content and quality by over-expressing artificially synthetic fusion proteins with high lysine and threonine constituent in rice plants. Sci. Rep. 6, 34427. Jin, W., Wu, F., 2016. Proteome-wide identification of lysine succinylation in the proteins of tomato (Solanum lycopersicum). PLoS One. 11, e0147586. Kang, P.T., Chen, C.L., Lin, P., Zhang, L., Zweier, J.L., Chen, Y.R., 2018. Mitochondrial complex I in the postischemic heart: reperfusion-mediated oxidative injury and protein cysteine sulfonation. J. Mol. Cell. Cardiol. 121, 190
204. Katagiri, F., 2004. A global view of defense gene expression regulation—a highly interconnected signaling network. Curr. Opin. Plant Biol. 7, 506
511. Kawamura, Y., Uemura, M., 2003. Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J. 36, 141
154. Kazan, K., 2015. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci. 20 (4), 219
229. Khan, K., Agarwal, P., Shanware, A., Sane, V.A., 2015a. Heterologous expression of two Jatropha aquaporins imparts drought and salt tolerance and improves seed viability in transgenic Arabidopsis thaliana. PLoS One 10 (6), 0128866. Khan, M.S., Ahmad, D., Khan, M.A., 2015b. Utilization of genes encoding osmoprotectants in transgenic plants for enhanced abiotic stress tolerance. Electron. J. Biotechnol. 18 (4), 257
266. Khare, T., Kumar, V., Kishor, P.K., 2015. Na1 and Cl2 ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma 252 (4), 1149
1165. Kim, J.I., Baek, D., Park, H.C., Chun, H.J., Oh, D.H., Lee, M.K., et al., 2013. Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. Mol. Plant 6, 337
349.

Plant Life under Changing Environment

536

20. Proteomics in relation to abiotic stress tolerance in plants

Komatsu, S., Deschamps, T., Hiraga, S., Kato, M., Chiba, M., Hashiguchi, A., et al., 2011. Characterization of a novel flooding stress-responsive alcohol dehydrogenase expressed in soybean roots. Plant Mol. Biol. 77, 309
322. Krishna, P., Prasad, B.D., Rahman, T., 2017. Brassinosteroid action in plant abiotic stress tolerance. Brassinosteroids. Humana Press, New York, pp. 193
202. Kumar, B., Singla-Pareek, S.L., Sopory, S.K., 2010. Glutathione homeostasis: crucial for abiotic stress tolerance in plants. In: Pareek, A., Sopory, S.K., Bohnert, H.J., Govindjee (Eds.), Abiotic Stress Adaptation in Plants. Springer, Dordrecht, The Netherlands, pp. 263
282. Kumar, R., Kumar, A., Subba, P., Gayali, S., Barua, P., Chakraborty, S., et al., 2014. Nuclear phosphoproteome of developing chickpea seedlings (Cicer arietinum L.) and protein-kinase interaction network. J. Proteomics 105, 58
73. Kumar, K., Mosa, K.A., Meselhy, A.G., Dhankher, O.P., 2018. Molecular insights into the plasma membrane intrinsic proteins roles for abiotic stress and metalloids tolerance and transport in plants. Indian J. Plant Physiol. 23, 721
730. Kume, S., Kobayashi, F., Ishibashi, M., Ohno, R., Nakamura, C., Takumi, S., 2005. Differential and coordinated expression of Cbf and Cor/Lea genes during long-term cold acclimation in two wheat cultivars showing distinct levels of freezing tolerance. Genes Genet. Syst. 80, 185
197. Kunkel, B.N., Brooks, D.M., 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325
331. Lake, I.R., Hooper, L., Abdelhamid, A., Bentham, G., Boxall, A.B.A., Draper, A., et al., 2012. Climate change and food security: health impacts in developed countries. Environ. Health Perspect. 120, 1520
1526. Available from: https://doi.org/10.1289/ehp.1104424. Lee, H.G., Seo, P.J., 2015. The MYB 96
HHP module integrates cold and abscisic acid signaling to activate the CBF
COR pathway in Arabidopsis. Plant J. 82 (6), 962
977. Lee, J.H., Yoon, H.J., Terzaghi, W., Martinez, C., Dai, M., Li, J., et al., 2010. DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 22, 1716
1732. Li, H., Yan, S., Zhao, L., Tan, J., Zhang, Q., Gao, F., et al., 2014. Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol. 14, 105. Li, X., Tan, D.X., Jiang, D., Liu, F., 2016. Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley. J. Pineal Res. 61 (3), 328
339. Liang, D., Liu, M., Hu, Q., He, M., Qi, X., Xu, Q., 2015. Identification of differentially expressed genes related to aphid resistance in cucumber (Cucumis sativus L.). Sci. Rep. 5, 9645. Lin, M., Gessmann, D., Naveed, H., Liang, J., 2016. Outer membrane protein folding and topology from a computational transfer free energy scale. J. Am. Chem. Soc. 138 (8), 2592
2601. Ling, Q., Jarvis, P., 2015. Regulation of chloroplast protein import by the ubiquitin E3 ligase SP1 is important for stress tolerance in plants. Curr. Biol. 25 (19), 2527
2534. Liu, H., Stone, S.L., 2010. Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell 22, 2630
2641. Liu, C., Li, S., Yue, J., Xiao, W., Zhao, Q., Zhu, D., et al., 2015. Microtubule-associated protein SBgLR facilitates storage protein deposition and its expression leads to lysine content increase in transgenic maize endosperm. Int. J. Mol. Sci. 16 (12), 29772
29786. Luo, M., Liu, X., Singh, P., Cui, Y., Zimmerli, L., Wu, K., 2012. Chromatin modifications and remodeling in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 129
136. Ma, Q.J., Sun, M.H., Kang, H., Lu, J., You, C.X., Hao, Y.J., 2018. A CIPK protein kinase targets sucrose transporter MdSUT2.2 at Ser254 for phosphorylation to enhance salt tolerance. Plant Cell Environ 42, 918
930. Madian, A.G., Regnier, F.E., 2010. Proteomic identification of carbonylated proteins and their oxidation sites. J. Proteome Res. 9, 3766
3780. Magome, H., Yamaguchi, S., Hanada, A., Kamiya, Y., Oda, K., 2008. The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J. 56, 613
626. Mahalingam, R., Gomez-Buitrago, A., Eckardt, N., et al., 2003. Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol. 4, R20. Mahrez, W., Arellano, M.S., Moreno-Romero, J., Nakamura, M., Shu, H., Nanni, P., et al., 2016. H3K36ac is an evolutionary conserved plant histone modification that marks active genes. Plant Physiol. 170, 1566
1577.

Plant Life under Changing Environment

References

537

Manzano, S., Martı´nez, C., Megı´as, Z., Go´mez, P., Garrido, D., Jamilena, M., 2011. The role of ethylene and brassinosteroids in the control of sex expression and flower development in Cucurbita pepo. Plant Growth Regul. 65 (2), 213
221. Margutti, M.P., Reyna, M., Meringer, M.V., Racagni, G.E., Villasuso, A.L., 2017. Lipid signalling mediated by PLD/PA modulates proline and H2O2 levels in barley seedlings exposed to short-and long-term chilling stress. Plant Physiol. Biochem. 113, 149
160. Martinez, V., Nieves-Cordones, M., Lopez-Delacalle, M., Rodenas, R., Mestre, T.C., Garcia-Sanchez, F., et al., 2018. Tolerance to stress combination in tomato plants: New insights in the protective role of melatonin. Molecules 23 (3), 535. Matamoros, M.A., Kim, A., Pen˜uelas, M., Ihling, C., Griesser, E., Hoffmann, R., et al., 2018. Protein carbonylation and glycation in legume nodules. Plant Physiol. 177 (4), 1510
1528. Mata-Pe´rez, C., Spoel, S.H., 2019. Thioredoxin-mediated redox signalling in plant immunity. Plant Sci. 279, 27
33. Maurel, C., Boursiac, Y., Luu, D.T., Santoni, V., Shahzad, Z., Verdoucq, L., 2015. Aquaporins in plants. Physiol. Rev. 95 (4), 1321
1358. McNeilly, D., Schofield, A., Stone, S.L., 2018. Degradation of the stress-responsive enzyme formate dehydrogenase by the RING-type E3 ligase Keep on Going and the ubiquitin 26S proteasome system. Plant Mol. Biol. 96 (3), 265
278. Mega, T., 2005. Glucose trimming of N-glycan in endoplasmic reticulum is indispensable for the growth of Raphanus sativus seedling (kaiware radish). Biosci. Biotechnol. Biochem. 69, 1353
1364. Mehrotra, R., Bhalothia, P., Bansal, P., Basantani, M.K., Bharti, V., Mehrotra, S., 2014. Abscisic acid and abiotic stress tolerance
different tiers of regulation. J. Plant Physiol. 171, 486
496. Available from: https://doi.org/ 10.1016/j.jplph.2013.12.007. Mickelbart, M.V., Hasegawa, P.M., Bailey-Serres, J., 2015. Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat. Rev. Genet. 16 (4), 237. Miller, C.J., Turk, B.E., 2018. Homing in: mechanisms of substrate targeting by protein kinases. Trends Biochem. Sci. 43, 380
394. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M.A., Shulaev, V., et al., 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45. 54, 848
858. Miller, D.J., Zhang, Y.M., Subramanian, C., Rock, C.O., White, S.W., 2010. Structural basis for the transcriptional regulation of membrane lipid homeostasis. Nat. Struct. Mol. Biol. 17 (8), 971. Miller, S.B., Mogk, A., Bukau, B., 2015. Spatially organized aggregation of misfolded proteins as cellular stress defense strategy. J. Mol. Biol. 427 (7), 1564
1574. Mittal, S., Mallikarjuna, M.G., Rao, A.R., Jain, P.A., Dash, P.K., Thirunavukkarasu, N., 2017. Comparative analysis of CDPK family in maize, Arabidopsis, rice, and sorghum revealed potential targets for drought tolerance improvement. Front. Chem. 5, 115. Mittler, R., 2017. ROS are good. Trends Plant Sci. 221, 11
19. Mock, H.P., Dietz, K.J., 2016. Redox proteomics for the assessment of redox-related posttranslational regulation in plants. Biochim. Biophys. Acta (BBA), Proteins Proteomics 1864 (8), 967
973. Mortimer, J.C., Laohavisit, A., Macpherson, N., Webb, A., Brownlee, C., Battey, N.H., et al., 2008. Annexins: Multifunctional components of growth and adaptation. J. Exp. Bot. 59, 533
544. Mun, B.G., Lee, S.U., Hussain, A., Kim, H.H., Rolly, N.K., Jung, K.H., et al., 2018. S-nitrosocysteine-responsive genes modulate diverse regulatory pathways in Oryza sativa: a transcriptome profiling study. Funct. Plant Biol. 45 (6), 630
644. Mustafa, G., Komatsu, S., 2014. Quantitative proteomics reveals the effect of protein glycosylation in soybean root under flooding stress. Front Plant Sci. 5, 627. Nahar, K., Rahman, M., Hasanuzzaman, M., Alam, M.M., Rahman, A., Suzuki, T., et al., 2016. Physiological and biochemical mechanisms of spermine-induced cadmium stress tolerance in mung bean (Vigna radiata L.) seedlings. Environ. Sci. Pollut. Res 23 (21), 21206
21218. Nallamilli, B.R., Edelmann, M.J., Zhong, X., Tan, F., Mujahid, H., Zhang, J., et al., 2014. Global analysis of lysine acetylation suggests the involvement of protein acetylation in diverse biological processes in rice (Oryza sativa). PLoS One 9, e89283. Netto, L.E., Antunes, F., 2016. The roles of peroxiredoxin and thioredoxin in hydrogen peroxide sensing and in signal transduction. Mol. Cells 39 (1), 65.

Plant Life under Changing Environment

538

20. Proteomics in relation to abiotic stress tolerance in plants

Neumann, P., Schubert, V., Fukova´, I., Manning, J.E., Houben, A., Macas, J., 2016. Epigenetic histone marks of extended meta-polycentric centromeres of Lathyrus and Pisum chromosomes. Front. Plant Sci. 7, 234. Ng, L.M., Melcher, K., Teh, B.T., Xu, H.E., 2014. Abscisic acid perception and signaling: structural mechanisms and applications. Acta Pharmacol. Sin. 35, 567
584. Available from: https://doi.org/10.1038/aps.2014.5. Nohzadeh Malakshah, M.S., Habibi Rezaei, M., Heidari, M., Salekdeh, G.H., 2007. Proteomics reveals new salt responsive proteins associated with rice plasma membrane. Biosci. Biotechnol. Biochem. 71, 2144
2154. Nouri, M.Z., Komatsu, S., 2013. Subcellular protein overexpression to develop abiotic stress tolerant plants. Front. Plant Sci. 4, 2. Ohama, N., Sato, H., Shinozaki, K., Yamaguchi-Shinozaki, K., 2017. Transcriptional regulatory network of plant heat stress response. Trends Plant Sci. 22 (1), 53
65. Oliveira-Ferrer, L., Legler, K., Milde-Langosch, K., 2017. Role of protein glycosylation in cancer metastasis, Seminars in Cancer Biology, 44. Academic Press, pp. 141
152. ¨ ktem, H.A., 2015. Functional role of nitric oxide under abiotic stress condiOz, M.T., Eyidogan, F., Yucel, M., O tions. Nitric Oxide Action in Abiotic Stress Responses in Plants. Springer, Cham, pp. 21
41. Pandey, A.K., Gautam, A., Dubey, R.S., 2019. Transport and detoxification of metalloids in plants in relation to plant metalloid tolerance. Plant Gene 17, 100171. Available from: https://doi.org/10.1016/j. plgene.2019.100171. Park, H.C., Park, C.Y., Koo, S.C., Cheong, M.S., Kim, K.E., Kim, M.C., et al., 2010. AtCML8, a calmodulin-like protein, differentially activating CaM-dependent enzymes in Arabidopsis thaliana. Plant Cell Rep. 29, 1297
1304. Petrov, V., Hille, J., Mueller-Roeber, B., Gechev, T.S., 2015. ROS-mediated abiotic stress-induced programmed cell death in plants. Front. Plant Sci. 6, 69. Pokhilko, A., Ramos, J.A., Holtan, H., Maszle, D.R., Khanna, R., Millar, A.J., 2011. Ubiquitin ligase switch in plant photomorphogenesis: a hypothesis. J. Theor. Biol. 270, 31
41. Pou, A., Medrano, H., Flexas, J., Tyerman, S.D., 2013. A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering. Plant Cell Environ. 36 (4), 828
843. Ranty, B., Aldon, D., Cotelle, V., Galaud, J.P., Thuleau, P., Mazars, C., 2016. Calcium sensors as key hubs in plant responses to biotic and abiotic stresses. Front. Plant Sci. 7, 327. Rao, S.S.R., Vardhini, B.V., Sujatha, E., Anuradha, S., 2002. Brassinosteroids
new class of phytohormones. Curr. Sci. 82, 1239
1245. Rao, V., Prakash, B.P., Verma, P., Salvi, P., Uttam, K.N., Ghosh, S., et al., 2018. Arabidopsis SKP1-like protein13 (ASK13) positively regulates seed germination and seedling growth under abiotic stresses. J. Exp. Bot. 69, 3899
3915. Reczek, C.R., Chandel, N.S., 2015. ROS-dependent signal transduction. Curr. Opin. Cell Biol. 33, 8
13. Reddy, A.S., Ali, G.S., Celesnik, H., Day, I.S., 2011. Coping with stresses: roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell 23 (6), 2010
2032. Rehman, S., Mahmood, T., 2015. Functional role of DREB and ERF transcription factors: regulating stressresponsive network in plants. Acta Physiol. Plant. 37 (9), 178. Reis, P.A., Carpinetti, P.A., Freitas, P.P., Santos, E.G., Camargos, L.F., Oliveira, I.H., et al., 2016. Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants. BMC Plant Biol. 16, 156. Riechmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C., Keddie, J., et al., 2000. Arabidopsis transcription factor: genome wide comparative analysis among eukaryotes. Science 290, 2105
2110. Robertson, E.J., Battigelli, A., Proulx, C., Mannige, R.V., Haxton, T.K., Yun, L., et al., 2016. Design, synthesis, assembly, and engineering of peptoid nanosheets. Acc. Chem. Res. 49 (3), 379
389. Rodrı´guez-Sanz, H., Moreno-Romero, J., Solı´s, M.T., Ko¨hler, C., Risuen˜o, M.C., Testillano, P.S., 2014. Changes in histone methylation and acetylation during microspore reprogramming to embryogenesis occur concomitantly with BnHKMT and BnHAT expression and are associated with cell totipotency, proliferation, and differentiation in Brassica napus. Cytogenet. Genome Res. 143, 209
218. Rout, G.R., Panigrahi, J., 2015. Analysis of signaling pathways during heavy metal toxicity: a functional genomics perspective. Elucidation of Abiotic Stress Signaling in Plants. Springer, New York, pp. 295
322. Rushton, P.J., Somssich, I.E., Ringler, P., Shen, Q.J., 2010. WRKY transcription factors. Trends Plant Sci. 15, 247
258.

Plant Life under Changing Environment

References

539

Ryu, H., Cho, Y.G., 2015. Plant hormones in salt stress tolerance. J. Plant Biol. 58 (3), 147
155. Sanei, M., Pickering, R., Fuchs, J., Banaei Moghaddam, A.M., Dziurlikowska, A., Houben, A., 2010. Interspecific hybrids of Hordeum marinum ssp. marinum x H. bulbosum are mitotically stable and reveal no gross alterations in chromatin properties. Cytogenet. Genome Res. 129, 110
116. Sanyal, S.K., Rao, S., Mishra, L.K., Sharma, M., Pandey, G.K., 2016. Plant stress responses mediated by CBL-CIPK phosphorylation network. Enzymes 40, 31
64. Savvides, A., Ali, S., Tester, M., Fotopoulos, V., 2016. Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci. 21 (4), 329
340. Seo, K.I., Lee, J.H., Nezames, C.D., Zhong, S., Song, E., Byun, M.O., Deng, X.W., 2014. ABD1 is an Arabidopsis DCAF substrate receptor for CUL4-DDB1
based E3 ligases that acts as a negative regulator of abscisic acid signaling. The Plant Cell 26 (2), 695
711. Shannon, D.A., Weerapana, E., 2015. Covalent protein modification: the current landscape of residue-specific electrophiles. Curr. Opin. Chem. Biol. 24, 18
26. Sharma, N., 2016. Antioxidant Response to Salt Stress in Rice Cultivars (Doctoral dissertation). Punjab Agricultural University, Ludhiana. Sharma, G., Giri, J., Tyagi, A.K., 2015. Rice OsiSAP7 negatively regulates ABA stress signalling and imparts sensitivity to water-deficit stress in Arabidopsis. Plant Sci. 237, 80
92. Shelden, M.C., Roessner, U., Sharp, R.E., Tester, M., Bacic, A., 2013. Genetic variation in the root growth response of barley genotypes to salinity stress. Funct. Plant Biol. 40, 516
530. Available from: https://doi.org/10.1371/ journal.pone.0022938. Shi, H., Ye, T., Yang, F., Chan, Z., 2015. Arabidopsis PED2 positively modulates plant drought stress resistance. JIPB 57 (9), 796
806. Simontacchi, M., Galatro, A., Ramos-Artuso, F., Santa-Marı´a, G.E., 2015. Plant survival in a changing environment: the role of nitric oxide in plant responses to abiotic stress. Front. Plant Sci. 6, 977. Singh, D., Laxmi, A., 2015. Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Front. Plant Sci. 6, 895. Singh, K., Foley, R.C., Onate-Sanchez, L., 2002. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 5, 430
436. Singh, D., Yadav, N.S., Tiwari, V., Agarwal, P.K., Jha, B., 2016. A SNARE-like superfamily protein SbSLSP from the halophyte Salicornia brachiata confers salt and drought tolerance by maintaining membrane stability, K1 / Na1 ratio, and antioxidant machinery. Front. Plant Sci. 7, 737. Smakowska, E., Blaszczyk, R.S., Czarna, M., Kolodziejczak, M., Kwasniak-Owczarek, M., Parys, K., et al., 2016. Lack of FTSH4 protease affects protein carbonylation, mitochondrial morphology and phospholipid content in mitochondria of Arabidopsis: new insights into a complex interplay. Plant Physiol. 171, 2516
2535. Smith-Hammond, C.L., Swatek, K.N., Johnston, M.L., Thelen, J.J., Miernyk, J.A., 2014. Initial description of the developing soybean seed protein Lys-N(ε)-acetylome. J. Proteomics 96, 56
66. Sonah, H., Deshmukh, R.K., Labbe´, C., Be´langer, R.R., 2017. Analysis of aquaporins in Brassicaceae species reveals high-level of conservation and dynamic role against biotic and abiotic stress in canola. Sci. Rep. 7 (1), 2771. Speiser, A., Silbermann, M., Dong, Y., Haberland, S., Uslu, V.V., Wang, S., et al., 2018. Sulfur partitioning between glutathione and protein synthesis determines plant growth. Plant Physiol. 177 (3), 927
937. Sponsel, V.M., Hedden, P., 2004. Gibberellin, biosynthesis and inactivation. In: Davies, P.J. (Ed.), Plant Hormones Biosynthesis, Signal Transduction, Action!. Springer, Dordrecht, pp. 63
94. Sreenivasulu, N., Sopory, S.K., Kavi, Kishor, P.B., 2007. Deciphering the regulatory mechanisms of abiotic stress tolerance in plants by genomic approaches. Gene 388, 1
13. Srivastava, V., Obudulu, O., Bygdell, J., Lo¨fstedt, T., Ryde´n, P., Nilsson, R., et al., 2013. On PLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI-superoxide dismutase Populus plants. BMC Genomics 14, 893. Available from: https://doi. org/10.1186/1471-2164-14-893. Stro¨her, E., Grassl, J., Carrie, C., Fenske, R., Whelan, J., Millar, A.H., 2016. Glutaredoxin S15 is involved in Fe-S cluster transfer in mitochondria influencing lipoic acid-dependent enzymes, plant growth, and arsenic tolerance in Arabidopsis. Plant Physiol. 170 (3), 1284
1299. Sze, H., Chanroj, S., 2018. Plant endomembrane dynamics: Studies of K1 /H1 antiporters provide insights on the effects of pH and ion homeostasis. Plant Physiol. 177 (3), 875
895.

Plant Life under Changing Environment

540

20. Proteomics in relation to abiotic stress tolerance in plants

Takemoto-Kimura, S., Suzuki, K., Horigane, S.I., Kamijo, S., Inoue, M., Sakamoto, M., et al., 2017. Calmodulin kinases: essential regulators in health and disease. J. Neurochem. 141 (6), 808
818. Tanou, G., Job, C., Rajjou, L., Arc, E., Belghazi, M., Diamantidis, G., et al., 2009. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J. 60, 795
804. Tognetti, V.B., Van Aken, O., Morreel, K., et al., 2010. Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22, 2660
2679. Tognetti, V.B., Mu¨hlenbock, P.E.R., Van Breusegem, F., 2012. Stress homeostasis
the redox and auxin perspective. Plant Cell. Environ. 35 (2), 321
333. Tripathi, P., Rabara, R.C., Reese, R.N., Miller, M.A., Rohila, J.S., Subramanian, S., et al., 2016. A toolbox of genes, proteins, metabolites and promoters for improving drought tolerance in soybean includes the metabolite coumestrol and stomatal development genes. BMC Genomics 17 (1), 102. Udawat, P., Jha, R.K., Sinha, D., Mishra, A., Jha, B., 2016. Overexpression of a cytosolic abiotic stress responsive universal stress protein (SbUSP) mitigates salt and osmotic stress in transgenic tobacco plants. Front. Plant Sci. 7, 518. Ullevig, S.L., Kim, H.S., Short, J.D., Tavakoli, S., Weintraub, S.T., Downs, K., et al., 2016. Protein S-glutathionylation mediates macrophage responses to metabolic cues from the extracellular environment. Antioxid. Redox Signal. 25 (15), 836
851. Upadhyay, R.K., Gupta, A., Soni, D., Garg, R., Pathre, U.V., Nath, P., et al., 2017. Ectopic expression of a tomato DREB gene affects several ABA processes and influences plant growth and root architecture in an agedependent manner. J. Plant Physiol. 214, 97
107. Usman, M.G., Rafii, M.Y., Ismail, M.R., Malek, M.A., Latif, M.A., 2015. Expression of target gene Hsp70 and membrane stability determine heat tolerance in chili pepper. J. Am. Soc. Hortic. Sci. 140 (2), 144
150. Vardhini, B.V., 2012. Application of brassinolide mitigates saline stress of certain metabolites of sorghum grown in Karaikal. J. Phytol. 4, 1
3. Vardhini, B.V., Anuradha, S., Rao, S.S.R., 2006. Brassinosteroids-new class of plant hormone with potential to improve crop productivity. Indian J. Plant Physiol. 11 (1), 1. Verma, V., Ravindran, P., Kumar, P.P., 2016. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 16 (1), 86. Vierstra, R.D., 2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385
397. Vinocur, B.J., Ayal, S., Diber, A., Emmanuel, E., Ronen, G., Gang, M., et al., 2017. Isolated Polypeptides and Polynucleotides Useful for Increasing Nitrogen Use Efficiency, Abiotic Stress Tolerance, Yield and Biomass in Plants. U.S. Patent Application15/673,608. Virdi, A.S., Singh, S., Singh, P., 2015. Abiotic stress responses in plants: roles of calmodulin-regulated proteins. Front. Plant Sci. 6, 809. Vishwakarma, K., Upadhyay, N., Kumar, N., Yadav, G., Singh, J., Mishra, R.K., et al., 2017. Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant Sci. 20 (8), 161. Wang, W., Vignani, R., Scali, M., Sensi, E., Cresti, M., 2004. Post-translational modifications of α-tubulin in Zea mays L. are highly tissue specific. Planta 218, 460
465. Wang, W., Gao, T., Chen, J., Yang, J., Huang, H., Yu, Y., 2019. The late embryogenesis abundant gene family in tea plant (Camellia sinensis): genome-wide characterization and expression analysis in response to cold and dehydration stress. Plant Physiol. Biochem. 135, 277
286. Wani, S.H., Kumar, V., Shriram, V., Shah, S.K., 2016. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J. 4 (3), 162
176. Waszczak, C., Akter, S., Jacques, S., Huang, J., Messens, J., Van Breusegem, F., 2015. Oxidative post-translational modifications of cysteine residues in plant signal transduction. J. Exp. Bot. 66 (10), 2923
2934. Waterland, N.L., Campbell, C.A., Finer, J.J., Jones, M.L., 2010. Abscisic acid application enhances drought stress tolerance in bedding plants. Hortic. Sci. 45, 409
413. Wimalasekera, R., Scherer, G.F., 2018. Involvement of mitogen-activated protein kinases in abiotic stress responses in plants. In: Plant Metabolites and Regulation Under Environmental Stress, pp. 389
395. Academic in Press, Elsevier.

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Further reading

541

Wu, Z., Zhao, X., Sun, X., Tan, Q., Tang, Y., Nie, Z., et al., 2015. Xylem transport and gene expression play decisive roles in cadmium accumulation in shoots of two oilseed rape cultivars (Brassica napus). Chemosphere 119, 1217
1223. Xia, X.J., Huang, L.F., Zhou, Y.H., Mao, W.H., Shi, K., Wu, J.X., et al., 2009. Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230 (6), 1185. Xiong, Y., Peng, X., Cheng, Z., Liu, W., Wang, G.L., 2016. A comprehensive catalog of the lysine-acetylation targets in rice (Oryza sativa) based on proteomic analyses. J. Proteomics 138, 20
29. Yadav, A.K., Jha, S.K., Sanyal, S.K., Luan, S., Pandey, G.K., 2018. Arabidopsis calcineurin B-like proteins differentially regulate phosphorylation activity of CBL-interacting protein kinase 9. Biochem. J. 475 (16), 2621
2636. Yin, X., Liang, X., Zhang, R., Yu, L., Xu, G., Zhou, Q., et al., 2015. Impact of phenanthrene exposure on activities of nitrate reductase, phosphoenolpyruvate carboxylase, vacuolar H1-pyrophosphatase and plasma membrane H1-ATPase in roots of soybean, wheat and carrot. Environ. Exp. Bot. 113, 59
66. You, J., Chan, Z., 2015. ROS regulation during abiotic stress responses in crop plants. Front. Plant Sci. 6, 1092. Yu, B., Li, J., Koh, J., Dufresne, C., Yang, N., Qi, S., et al., 2016. Quantitative proteomics and phosphoproteomics of sugar beet monosomic addition line M14 in response to salt stress. J. Proteomics 143, 286
297. Zaffagnini, M., Bedhomme, M., Groni, H., Marchand, C.H., Puppo, C., Gontero, B., et al., 2012. Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey. Mol. Cell. Prot. 11 (2), M111
014142. Zaffagnini, M., Bedhomme, M., Marchand, C.H., Couturier, J., Gao, X.H., Rouhier, N., et al., 2012. Glutaredoxin s12: unique properties for redox signaling. Antioxid. Redox. Sign. 16 (1), 17
32. Zandalinas, S.I., Mittler, R., Balfago´n, D., Arbona, V., Go´mez-Cadenas, A., 2018. Plant adaptations to the combination of drought and high temperatures. Physiol. Plant. 162, 1. Zargar, S.M., Nagar, P., Deshmukh, R., Nazir, M., Wani, A.A., Masoodi, K.Z., et al., 2017. Aquaporins as potential drought tolerance inducing proteins: towards instigating stress tolerance. J. Proteomics 169, 233
238. Zeng, H., Xu, L., Singh, A., Wang, H., Du, L., Poovaiah, B.W., 2015. Involvement of calmodulin and calmodulinlike proteins in plant responses to abiotic stresses. Front. Plant Sci. 6, 600. Zhang, Z., Tan, M., Xie, Z., Dai, L., Chen, Y., Zhao, Y., 2011. Identification of lysine succinylation as a new posttranslational modification. Nat. Chem. Biol. 7, 58
63. 75. Zhang, L., Zhang, L., Xia, C., Zhao, G., Liu, J., Jia, J., et al., 2015. A novel wheat bZIP transcription factor, TabZIP60, confers multiple abiotic stress tolerances in transgenic Arabidopsis. Physiol. Plant. 153 (4), 538. Zhang, Y., Song, L., Liang, W., Mu, P., Wang, S., Lin, Q., 2016. Comprehensive profiling of lysine acetylproteome analysis reveals diverse functions of lysine acetylation in common wheat. Sci. Rep. 6, 21069. Zhang, S., Gao, M.R., Fu, H.Y., Wang, X.M., Ren, Z.A., Chen, G.F., 2018. Electric Field Induced Permanent Superconductivity in Layered Metal Nitride Chlorides HfNCl and ZrNCl. Chinese Phys. Lett. 35 (9), 097401. Zhao, B., Fan, B., Shao, G., Zhao, W., Zhang, R., 2015. Facile synthesis of novel heterostructure based on SnO2 nanorods grown on submicron Ni walnut with tunable electromagnetic wave absorption capabilities. ACS Appl. Mater. Interfaces 7 (33), 18815
18823. Zhen, S., Deng, X., Wang, J., Zhu, G., Cao, H., Yuan, L., et al., 2016. First comprehensive proteome analyses of lysine acetylation and succinylation in seedling leaves of Brachypodium distachyon L. Sci. Rep. 6, 31576. Zhong, X., Zhang, H., Zhao, Y., Sun, Q., Hu, Y., Peng, H., et al., 2013. The rice NAD 1 -dependent histone deacetylase OsSRT1 targets preferentially to stress- and metabolism-related genes and transposable elements. PLoS One 8, e66807. Zhu, J.K., 2016. Abiotic stress signaling and responses in plants. Cell 167 (2), 313
324. Zhu, M., Shabala, L., Cuin, T.A., Huang, X., Zhou, M., Munns, R., et al., 2015. Nax loci affect SOS1-like Na1 /H1 exchanger expression and activity in wheat. J. Exp. Bot. 67 (3), 835
844. Zo¨rb, C., Schmitt, S., Mu¨hling, K.H., 2010. Proteomic changes in maize roots after short-term adjustment to saline growth conditions. Proteomics 10, 4441
4449.

Further reading Mendes, L.F., Tam, W.L., Chai, Y.C., Geris, L., Luyten, F.P., Roberts, S.J., 2016. Combinatorial analysis of growth factors reveals the contribution of bone morphogenetic proteins to chondrogenic differentiation of human periosteal cells. Tissue Eng. C: Methods 22 (5), 473
486.

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21 Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects Santwana Tiwari, Divya Gupta, Abreeq Fatima, Shikha Singh and Sheo Mohan Prasad Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, India

21.1 Introduction Plants are continuously under the influence of various environmental stresses that include biotic and abiotic stresses. Abiotic stresses are prevalent in present day’s plants because of several anthropogenic factors such as pollution and global warming and greenhouse gases. The rapidly increasing human population has worsened the crop production so there is a need for substantial increase in the agricultural productivity worldwide. Boyer (1982) noticed that up to 70% of the crop productivity is affected by environmental factors. The potential climatic abnormalities, such as global warming, have typically encountered an increased number of stresses that severely strike the maturation of the plants below optimum level. The abiotic stressors include intense degree of light (weak and intense), ultraviolet (UV) radiations, including both UV-B and UV-A, different measures of temperature (chilling or freezing), extent of water (flooding, drought, and submergence), various chemical factors (heavy metals, salinity, and pH), shortage or surplus of essential nutrients, gaseous pollutants of atmosphere (sulfur dioxide, ozone), and other minor, frequently occurring stressors. Among them, drought, temperature, and heat, which are categorized to be more devastating to crop production, also influence the occurrence and spread of insects, pathogens, and weeds (Coakley et al., 1999; Scherm and Coakley, 2003; Mittler, 2006; McDonald et al., 2009; Ziska et al., 2010; Peters et al., 2014). After drought, the second major stress that affects plant growth, pigment content, water relations, and the photosynthetic activity is salinity, which ultimately leads to loss of crop Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00024-2

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productivity (Sanghera et al., 2011; Pathak et al., 2014). Plant’s physiological activities and their definite responses are also being disturbed by pressure conditions that straightly affect plant
pest interactions. Moreover, most of the abiotic stress conditions intensify competitive interactions of weed on crops as many weeds have more water-holding capacity than crops (Ziska et al., 2010; Valerio et al., 2013). Due to difficulties of stress tolerance trait, the success rate of these traditional techniques is limited. So in order to meet the growing food demand worldwide, effective, novel, and potent approaches should be devised in this particular direction. Engineering of phytohormones could be a logical arrangement and a perfect platform to build the climate-resilient crops with high yields, which can also improve the crops nutritionally as well as economically. The phytohormones are known to be the ultimate powerful endogenic substances for hormonizing physiological and molecular responses in plants in their low concentrations. So in particular, in conditions when plants are subjected to stresses, their growth and development are regulated by them (Table 21.1). In higher plants, they work as chemical messengers for the fulfillment of the cellular activities. Growth and blossoming of plants must be regulated in order to retaliate against diverse external and internal stimuli. During abiotic stress response, the key role is played by phytohormones to coordinate several signal transduction pathways. Among the recognized categories of plant hormones, auxins, abscisic acid (ABA), cytokinins (CKs), gibberellins, ethylene (ET), jasmonic acid (JA), and strigolactones are the ones that have gathered most of the attention in the scientific world for their different physiological and morphological responses (Table 21.1). One of the phytohormones that has been recognized as a stress hormone is ABA. Besides various roles of arbitrating abiotic and biotic stress responses, ABA plays a pivotal role in the development of plants, continuation of seed dormancy, modulation of growth, inhibition of germination, abscission of young fruits, and stomatal closure. In response to salinity, Wang et al. (2001) stated that growth inhibiting hormones, such as ABA and JA, have increased, whereas growth promoting hormones, such as indole-3-acetic acid (IAA) and salicylic acid (SA), have decreased. So basically for upgrading the nutritional and economical values of crops, production of phytohormones could be a flawless platform for biotechnologists. Utmost important adaptations and stress responses in plants have been reported to be managed by phytohormones (Sharma et al., 2005; Shaterian et al., 2005). A significant decline in the endogenous level of phytohormones has also been seen due to unfavorable outcome of salinity on germination of seeds and plant growth (Zholkevich and Pustovoytova, 1993; Jackson, 1997; Debez et al., 2001). Consequently, their metabolic role grants abiotic stress tolerance in various vegetative crop plants to raise food quality and quantity. The area of action of phytohormones is either at their site of synthesis or in the transport processes in plants (Table 21.1). In this chapter we will be emphasizing the interactive role of phytohormones and their signaling behavior in order to ameliorate abiotic stress responses and increase the abiotic stress tolerance, food quality, and quantity among the crops. We will be discussing recent successes and their future perspective.

21.2 Phytohormone biosynthesis and signaling pathways All phytohormones exert different effects on the physiology of the plants, acting concomitantly in an orchestrated fashion, with an intricate network of signaling pathways, Plant Life under Changing Environment

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21.2 Phytohormone biosynthesis and signaling pathways

TABLE 21.1 Summary of major plant hormones: biological effects, metabolic precursors, production sites, and receptor responses. Phytohormones

Biosynthetic pathway

Precursor

Where produced in plants

Major functions

1. ABA

Isoprenoid pathway (carotenoid biosynthesis pathway)

IPP-derived tetra-terpene (phytoene)

Nearly all plant cells have the potential to synthesize ABA. The presence of ABA has been detected from every major organ and living tissues of plants

Plays role in closing of stomata under water stress, also modulates the potassium and sodium uptake within the guard cells, seed dormancy

2. Auxin (IAA)

Tryptophan biosynthetic pathway

Tryptophan

Young leaves and shoot apical meristems are major sites for auxin synthesis. Root apical meristem also known to produce auxin

Stimulates cell enlargement, bud formation, and root initiation. They are also known to promote other phytohormones’ production. With cytokinins, they control growth of stems, roots, and fruits, and convert stems into flowers. Function in gravitropism and phototropism

3. CKs

Isoprenoid pathway (zeatin biosynthesis)

Adenine

Predominantly they are synthesized in root tissues although, there are many minor sites for their production and then they are transported to other organs

Promotes lateral growth of buds and modifies the apical dominance. It regulates cell division in root and shoot. Also stimulates seed germination and delays senescence

4. BRs

Isoprenoid pathway (brassinosteroid biosynthetic pathway)

IPP-derived sesqui-terpene (farnesyl diphosphate)

Ubiquitous, that is, present in all plant tissues, internally produced act near site of synthesis

Brassinosteroids control cell elongation and division, gravitropism, resistance to stress, and xylem differentiation. They inhibit root growth and leaf abscission

5. ET

Ethylene biosynthetic pathway (cysteine and methionine metabolism)

Methionine

Can be produced by most parts of the plant. During leaf abscission and senescence, they are produced in high concentration. It is also reported that ET is produced at a faster rate in rapidly growing and dividing cells, especially in darkness

Triple response, that is, inhibition of stem elongation, promotion of lateral leaf expansion, and horizontal growth of seedling, enhances rate of senescence and promotes root, and root hair formation. Ethylene also plays a role in ripening of many types of fruits (Continued)

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TABLE 21.1 (Continued) Phytohormones

Biosynthetic pathway

Precursor

Where produced in plants

Major functions

6. GAs

Isoprenoid pathway

IPP-derived di-terpene (geranylgeranyl diphosphate)

Sites of their production are meristem tissues of apical bud and roots, young leaves and developing seeds, etc.

Plays role in germination of seeds and sprouting of buds. They strongly promote cell elongation, also promote the transition between vegetative and reproductive growth. They are also required for pollen function during fertilization and fruit development

7. JA

Linolenic acid pathway/ octadecanoid pathway (lipid metabolism)

Linolenic acid

Produced in several parts and moved to other parts of the plant through phloem

JAs are important in the plant response to attack from herbivores and necrotrophic pathogens. In addition to this, JAs are also believed to play roles in seed germination, the storage of protein in seeds, and root growth

8. SA

Phenylalanine metabolism

Chorismate

9. SLs

Isoprenoid pathway (carotenoid biosynthesis pathway)

Carotenoids

In plants, SA plays a critical role in the defense against biotrophic pathogens. It is also involved in the response of plants to various abiotic stresses In response to low phosphate condition, these compounds are produced in root or under high auxin flow, produced from shoots

Plays roles in leaf senescence, phosphate starvation response, salt tolerance, and light signaling, SLs also identified to cause inhibition of shoot branching.

ABA, Abscisic acid; BRs, brassinosteroids; CKs, cytokinins; ET, ethylene; GAs, gibberellins; JA, jasmonic acid; JAs, Jasmonates; SA, salicylic acid; SLs, strigolactones.

including the three pathways: (1) SA pathway, (2) JA pathway, and (3) brassinosteroid (BR) pathway, which are generally induced via the herbivory. How outputs from the jasmonates (JAs), SA, and BR signaling pathways are being integrated in the regulation of stress responses and plant development is also examined. These pathways are the first line of defense against any external damage to plants.

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21.2.1 Auxin Auxin is considered to be one of the most multifunctional phytohormones and a vital mediator of physiological and developmental responses (Table 21.1). Some other cellular functions, including depolarization of plasma membrane, apoplastic acidification, induction of lateral and adventitious roots, phototropic and gravitropic responses, are also being categorized under the major role of auxin. For the biotic and abiotic responses, auxin is considered as a significant constituent of defense responses by the synchronization of numerous genes (Fahad et al., 2015). For more than 100 years, auxin is being studied; its biosynthesis, transport, and signaling pathways, which modulate gene expression by affecting growth and regulation, are the paramount issues. The details of auxin biosynthesis are still difficult to figure out, but it is familiar that the amino acid tryptophan can be employed as a precursor (Cohen et al., 2003) in some interconnecting pathways that encompass four tryptophan-dependent and majorly one tryptophan-independent pathway (Mano and Nemoto, 2012). In the 1920s, for the transport of auxin, a chemiosmotic hypothesis was suggested by Cholodny and Went. This theory prognosticates about the presence of auxin efflux carrier proteins which on gravitropic or phototropic stimulation, redistribute auxin asymmetrically in root and stem tissues. In past decades, movement of auxin requires molecular components, namely, PIN and AUX1, which are called auxin efflux and influx transporters, respectively. (Bennett et al., 1996; Luschnig et al., 1998; Ga¨lweiler et al., 1998). The overall machinery of auxin transport in plant tissues is likely to be regulated by gradient formation. For example, in Arabidopsis, it has been reported that at root apex there is maximum auxin concentration that depends majorly on the activity of PIN4, and this gradient is sink driven (Friml et al., 2002). In the nucleus, some families of auxin induced proteins: the Aux/IAA protein and the auxin response factors (ARFs) are involved in the regulation of gene expression (Hagen and Guilfoyle, 2002). Subsequent analysis shows that transcription is activated or repressed by ARF that binds to upstream located auxin response promoter element. Aux/IAA protein inhibits the activity of ARF by dimerizing with it (Tiwari et al., 2003). ARF
Aux/IAA dimer has an inhibitory role on the auxin response, so its concentration is lowered by the speedy turnover of Aux/IAA protein (Worley et al., 2000). Aux/IAA proteins are categorized by four highly conserved domains that are mainly found in most of the higher plants (Guilfoyle et al., 1998). For the functioning of Aux/IAA, domain II plays a crucial role in protein destabilization and giving evidences to ensure a fast turnover for a regular auxin response. Luciferase (GUS) are the reporter proteins which get destabilized when get fused with Aux/IAA proteins; this clearly indicates the existence of destabilized sequence in Aux/IAA proteins (Worley et al., 2000; Gray et al., 2001). Many mutants, such as axr3-1, axr2-1, and shy2, are auxin resistance, which carry a nonfunctional domain II that has a two-way function— dramatically raising the half-life of proteins and consecutively averting the ARF proteins from functioning (Worley et al., 2000; Gray et al., 2001; Ouellet et al., 2001). However, many growing evidences depict inhibitors such as 26S proteasome that get fused by Aux/IAA reporter fusion and are involved in the stabilization, specifying that signaling of auxin demands SCFTIR1mediated turnover of Aux/IAA proteins. Importantly, these proteins straightly interact with the TIR1 subunit of the SCF/TIR1 complex, and thereafter with the demand of auxin, these

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interconnections are elevated, which leads to the degradation of Aux/IAA. These results clearly signify the participation of such ubiquitin-dependent degradation machinery in regard to auxin signaling, the location of which is found to be placed in the upstream of AUX/IAA, which is considered to be the transcriptional repressors (Dharmasiri et al., 2005a). Thus the consequence of auxin on gene expression is being mediated by many of the functional auxin receptors that involve TIR1 and a handful of related F-box proteins (Dharmasiri et al., 2005b). But up to now, many of the techniques of auxin signaling, physiological role of AUX/IAAs and ARFs, and their connection with each other are unclear.

21.2.2 Abscisic acid A variety of strategies are required for the plants to get adapted to the environmental challenges, the phytohormone ABA being one of them to control it. Among them, the mechanism to control water balance is very well regulated. Anatomy of leaves in most of the land plants is totally centered on how to balance diminishing the water loss and boosting the area for sun exposure. Due to this balance the electron flux that passes across the lightdependent reactions of photosynthesis is crucially retained. Evaporation causes loss of water from pores (stomata) due to the exposure of high intensity of light. Opening and closing of stomata are regulated by ABA to check the water loss. ABA responses are enhanced by many measures such as high salinity, drought, low temperature leading to physiological changes (gene articulation in reply to salinity and drought); it is required to get through such a disadvantageous state (Lee and Luan, 2012). Moreover, ABA also influences developmental processes by regulating area of the leaf, internode length, dormancy of seeds and bud, development and reproduction of embryo and seeds. With extensive study, it has been seen that a number of secondary messengers are involved in the signaling of ABA, which include lipid-derived signals, nitric oxide (NO), H2O2, and G-proteins (Himmelbach and Yang, 2003). Different concentration of these cellular compounds unite together and indirectly influence concentration of cytosolic Ca21, which is the prime ingredient in ABA signaling (McAinsh and Brownlee, 1997). Genomic, by altering the level of transcription of various ABA responsive genes involved, and nongenomic effects, by altering ion permeability of plasma membrane by changing the turgor pressure of guard cell, are the two most considered modes of action of ABA. Thoughtfully, with the variation of intracellular concentration of Ca21, both the processes are dependent, however, in what way these pathways are separated has not been fully understood. Despite having an extended history of research, the nature of initial ABA receptor is still elusive, but most of the events which occur at the inceptive level in the cascade of signaling is believed to be the binding of ABA to either membrane-bound or receptors present in the cytosol. Another important factor of this process involves intracellular signals that are derivative of lipid and cyclic-adenosine 50 diphosphate-ribose concentration, which first alters the Ca21 permeability of the tonoplast and latter Ca21 concentration itself engaged in the major role (Wu et al., 2003). Lastly, the net hike in intracellular Ca21 results in the activation of K1 efflux channels and holding back of both K1 influx and H1 adenosine triphosphatase channels. Thus a tangled mesh of interconnecting signals is initiated by ABA in response to various stresses resulting in physiological responses (Finkelstein et al., 2002).

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21.2.3 Brassinosteroids In plants as well as in animals, the steroids are the important signaling molecules which have a strong promoting potential for growth and development. BR, discovered in 1979, is a steroidal hormone whose polyhydroxy nature is categorized in a relatively new group which is involved in various developmental phases of a plant, such as germination, elongation of stem, and senescence. BRs are synthesized from cholesterol and thought to play an important role in photo-morphogenesis by an evidence of warf mutant de-etiolated2 (DET2) and BR related markers gene (CPD) that are lacking in the biosynthesis of BRs. Hence, they are considered as mutants, which when planted in dark looks like a lightgrown plant. This clearly defines the above point (Chory et al., 1991; Li and Chory, 1997). In the phytohormone biology, many of the BR receptors have been identified; this particular part focuses that the cells at the beginning sense the mechanism of BRs and some of the interesting similarities in the mode of action and perception of BRs. Studies show that in order to receive the BR signals, plants have achieved a different method, as in plants, steroid receptors are not located near the nucleus, but in animals, they are located inside the nucleus (Marcinkowska and Wiedlocha, 2002). Some of the Arabidopsis mutants, such as BR related markers gene (BRI), show a dwarf phenotype, same as reported in the mutant deficient in the BR biosynthesis. Mutant plants show unresponsiveness when there is an application of brassinolide; however, it was predicted that BRI1 was involved in the signaling section. Gene cloning of BRI1 shows the existence of a BR receptor which is an immediate candidate having leucine-rich repeat (LRR) with kinase-like receptor (Li and Chory, 1997). For the bioactive BR, BRI1 is believed to have a high affinity (Wang et al., 2001), and its position is being confirmed near the plasma membrane. There are three domains in the LRR-receptor kinase: a transmembrane domain, a cytoplasmic domain, and a domain having repeating leucine-rich sections, for example, BRI1, 25 whose location is extracellular. The LRR domain of BRI1 also encompasses an island of 70 amino acids for the function of protein (Li and Chory, 1997). The extracellular domain of BRI1, by using some of the chimeric protein, has justified that this domain is both requisite and adequate for the specific set of genes to be translated. Recent research has given an overview of the stupendous potential of BRs and other interconnecting compounds in reaction to and also to counteract the abiotic stress-induced oxidative burst by adjusting the components of the antioxidant system, as reviewed by Vardhini and Anjum (2015). This defense-related gene expression can be induced when the intracellular kinase domain gets fused with a related receptor such as kinase, an assemblage of proteins that gets involved in the activation of BRI1 extracellular domain, which activates a plant defensive response against pathogens (He et al., 2003). It has also been reported that Arabidopsis comprises 174 members, which form a very vast class of protein having LRR-receptor kinases related with diverse functions. Small functions are assigned, such as for CLAVATA that participates in the development of meristem and another being ERECTA that participates in organogenesis (Dievart and Clark, 2003). In monocotyledonous species, many protein sequences are found similar to three BRI-like proteins that share high homology to Arabidopsis. As BRI1 mutations have been rescued by BRL1 and BRL3, it suggests that they share close related function. In plants attacked by pathogens, the pathogen defense responses deal with the signal peptide known as systemin that works with JAs by boosting the introduction of the

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JAs signaling pathway. For the systemin and BR signaling it was discovered that the similar receptor (in state of systemin called SR160) was accountable (Montoya et al., 2002; Szekeres, 2003). Progesterone, being an animal hormone, also shows the same dual function of receptors as it is connected to the functions that involve hindering the peptide oxytocin chiefly from binding to its receptor, a G-protein-coupled receptor of uterine cavity (Grazzini et al., 1998). However, BRs are mainly involved in mitigating the impact of abiotic stresses, such as metals (Bajguz, 2010), light (Kurepin et al., 2012), chilling (Wang et al., 2014), drought (Mahesh et al., 2013), soil salinity (Abbas et al., 2013), and organic pollutants, which have been suggested in many of the recent findings. But much of the areas of BRs, such as their biosynthesis, source
sink relationship, stress physiology, and their developmental processes, are to be focused in future research in order to become aware of their powerful applications.

21.2.4 Cytokinin CKs play a major and an influential part in multiple plant growth and developmental processes (Table 21.1), the list of which completes with cell division, chloroplast development, leaf senescence, nutrient mobilization, pathogen resistance, and stress response by which CKs are considered as master regulators (Nishiyama et al., 2011; Kang et al., 2012). For the biosynthesis of this particular hormone CK, mainly two mechanisms have been hypothesized, first which will lead to tRNA CK and second which will lead to free CK. As certain tRNAs comprise CK, synthesis and yield of tRNA are the possible route to free CK formation. Evidences suggest that biosynthesis via tRNA may not be a prime source of CKs. It is possible that during active growth periods, in both root-and-shoot meristem, CKs are synthesized. It is also evident that long distance transport can be envisaged in case of root only, whereas CKs produced in shoot meristem are distributed to the tissue lying close to the site of production. A tagging experiment suggests that CK responses are induced by a gene present in Arabidopsis plant known as CKI1 which encodes a receptor histidine kinase (Kakimoto, 1996). Although CKI1 does not bind CK directly it is believed that it is able to turn on CK signaling pathway (Hwang and Sheen, 2001). By the finding of CKI1 it was noticed that in higher plants the transduction pathway of CK could be alike with the two-component system of prokaryotes. Evidences suggest that the above hypothesis was shown to be true with the recognition of the first CK receptor CRE1/AHK4 which acts as a histidine kinase (Inoue et al., 2001). Moreover two more CK receptors (AHK2 and AHK3) were identified in the genomic sequences of Arabidopsis. A multistep phosphorelay system transmits the resulting system through a complicated form of the two-component signaling pathways that has been very well demonstrated particularly in prokaryotes and also in lower eukaryotes. A number of experiments that were elegantly performed in yeast and Escherichia coli gave many of the evidences related to the functional aspects of the receptor CRE1/AHK4 that provides knowledge about the CK sensitive heterologous host. Two other proteins are also involved, namely, AHK2 and AHK3, which are histidine kinases, are active in the above-discussed complementation test system, and confirms the protoplast CK sensitivity pointing out that these two proteins additionally act as CK receptors (Hwang and

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Sheen, 2001). Each receptor encompasses two terminals: N-terminal, which is an extracellular domain and can perform autophosphorylation, and C-terminal, which is a transmitter domain and also contains a membrane anchor. If we consider these CK receptors, such as CRE1/AHK4, AHK2, and AHK3, which are also considered as histidine kinases, CRE1/AHK4 is majorly found in roots whereas in most of the organs AHK2 and AHK3 are present, but both of them greatly differ in their expression patterns (Inoue et al., 2001). According to the perception of CK, this tissue-specific aspect of CK could be an extra layer of control. Such cross talks between nutrients and CK as well as between CK and other phytohormones are very important to understand the growth responses to CK, which have been demonstrated in many of the studied data. Moreover, glucose repression responses are overcome by the proper application of CK and transgenic Arabidopsis lines with constitutive CK signaling. Much of the research also depicts that CKs are antagonistic to ABA (Pospı´sˇ ilova´, 2003). In water stressed plants, there is an enhancement in the level of ABA/CK ratio as CK content declines and ABA content gets accumulated. Due to this lower level of CK, apical dominance is escalated and simultaneously with the ABA modulation, results in the adaptation to drought stress (O’Brien and Benkova, 2013).

21.2.5 Gibberellic acid The hormone gibberellin constitutes a large group of diterpenoids such as carboxylic acids that are ubiquitously present in plants whose certain members function as endogenous growth regulators, promoting expansion of the organs and bringing about the developmental changes (Table 21.1). Gibberellic acid (GA) is synthesized in the actively growing regions of the plant. GA is formed from the methylerythritol phosphate pathway by which the hydrocarbon intermediate ent-kaurene is produced from GGPP (trans-geranylgeranyl diphosphate) in proplastids. It has been studied so far that ent-kaurene synthesis competes with other GGPS isozymes. The synthesis of ent-kaurene from GGPP mainly involves two steps via ent-copalyl diphosphate, and the reactions are catalyzed by different enzymes: ent-copalyl diphosphate synthase (CPS, a class II cyclase) and ent-kaurene synthase (KS, a class I cyclase). In higher plants, ent-kaurene is volatile in nature, hence it is found to exchange with the external environment functioning as a mediator of plant-toplant interaction and communication. The oxidation of ent-kaurenoic acid to GA12 by nt-kaurenoic acid oxidase (KAO) occurs in three consecutive steps via the intermediates ent-7α-hydroxykaurenoic acid and GA12-aldehyde, requiring successive oxidations at C-7β, C-6β, and C-7. GA12 and GA53 get oxidized on C-20 by GA20ox (GA 20-oxidase), an 2-oxoglutarate-dependent dioxygenases (ODD), which converts these substrates into two parallel pathways GA9 and GA20. The final step in the synthesis of the biologically active hormones is the 3β-hydroxylation of GA9 and GA20 to GA4 and GA1, respectively, catalyzed by the ODD GA3ox (GA 3-oxidase). Earlier biochemical studies on oat aleurone cells suggest that the GA signal is perceived by a receptor present in the plasma membrane (Lovegrove et al., 1998). But, it was recently when the characterization of the GA-insensitive dwarfism gid1-1 mutant allele in rice led to the discovery of the GA receptor, GID1 (Ueguchi-Tanaka et al., 2005). GA binding to

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GID1 stimulates the formation of the GA-GID1-DELLA complex and the GA stimulates the disappearance of DELLAs (Silverstone et al., 1997). Whereas in absence of GA, DELLAs get accumulated and repress the responses of GA, the formation of the GA-GID1-DELLA complex triggers the degradation of the DELLAs. As screened from the rice, GID2 and Arabidopsis signaling involves SLT1 F-box proteins which are the components of SCF (SKP1, CULLIN, F-BOX) E3 ubiquitin-ligase complexes, catalyzing the attachment of polyubiquitin chains to target other proteins for their successive degradation by the 26S proteasome (Lechner et al., 2006). In response to that, the SCFSLY1/GID2 complex promotes the ubiquitination and the subsequent destruction of DELLAs by 26S proteasome, therefore relieving their growth-restraining effects (McGinnis et al., 2003; Dill et al., 2004). Thus it is concluded that GA stimulates growth by harmonizing the proteasome-dependent destabilization of DELLA proteins. Surprisingly, few evidences also indicate that GA-mediated removal of DELLA proteins is required in a cell specific manner to ensure normal organ growth of the plant including flowering, leaf expansion, trichome, and pollen development.

21.2.6 Ethylene The hormone ET despite a simple two-carbon structure is a potent modulator of growth and development of the plant It is intricately involved in many aspects of the plant life cycle, including seed germination, root hair development, root nodulation, flower senescence, abscission, and fruit ripening. The synthesis and production of ET is very tightly regulated by internal signals and cues during development and in response to environmental stimuli such as biotic (e.g., pathogen attack) and abiotic stresses, wounding, hypoxia, ozone, chilling, or freezing. The biochemistry of ET synthesis has been a subject of debate in plant hormone physiology. Major breakthroughs and evidences of its biosynthesis come from the establishment of S-adenosylmethionine (S-AdoMet) and amino cyclopropane carboxylate (ACC) as the precursors of ET (Yang and Hoffman, 1984). On the basis of these evidences, enzymes catalyzing these reactions were characterized and purified using biochemical approaches. Primary successes in molecular cloning of the ACC synthase (ACS) (Sato and Theologis, 1989) and ACC oxidase (ACO) (Hamilton et al., 1991; Spanu et al., 1991) genes led to the demonstration that these enzymes belong to a multigene family and are regulated by a complex network of developmental and environmental signals which responds to both. Perception of ET is mediated by a family of five membrane-localized receptors which is homologous to bacterial two-component histidine kinases involved in sensing environmental changes. Epistatic analysis has placed CTR1 downstream of the ET receptors in the signaling pathway. Thus it is reported that CTR1 is a negative regulator of downstream signaling events of ET and it belongs to the Raf family of Ser/Thr protein kinases which initiates mitogen-activated protein (MAP)
kinase signaling cascades in mammals (Kyriakis et al., 1992). The similarity of CTR1 to known MAPKKKs signifies that ET signaling may operate via MAP-kinase cascade. Various other epistatic analyses of ET responsive mutants have shown that EIN2 acts downstream of CTR1 and upstream of EIN3. Mutations in EIN2 resulted in the complete loss of ET responsiveness throughout plant

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development which signifies that EIN2 is an essential component in regulating ET signaling pathway. These results suggest that the N-terminal portion of EIN2 is significant for sensing the ET signal from upstream components in the pathway, whereas EIN2 CEND is invariably required for transducing the signal to the downstream components. In addition to this, EIN2 mutants also show altered sensitivity to several bacterial and fungal pathogens.

21.2.7 Jasmonic acid Plant responses against various abiotic stresses are synchronized locally as well as systemically by signaling molecules called JAs. JAs are known to regulate many diverse processes such as pollen maturation and wound responses in Arabidopsis. The term JAs include the biologically active intermediates in the pathway of JA biosynthesis and other biologically active derivatives of JA. The systemic induction of JAs responses in tomato is through the well-characterized systemin signal pathway (Constabel et al., 1995), but no evidence for an equivalent pathway can be found in Arabidopsis, even though systemic signaling can be demonstrated (Kubigsteltig et al., 1999). JAs are a class of cyclic fatty acid
derived phytohormones that regulate various developmental and defense responses to biotic and abiotic stresses (Santino et al., 2013; Wang and Wu, 2013; Campos et al., 2014; Wasternack, 2014). JAs signaling can be induced by an array of abiotic stresses, which include osmotic stress (Kramell et al., 2000), drought, wounding, and exposure to other “elicitors,” such as chitin, oligosaccharides, oligogalaturonides (Doares et al., 1995), and extracts from yeast (Parchmann et al., 1997; Leon et al., 2001). During 1994
98, it was stated by US scientists Feys et al. (1994) and Vijayan et al. (1998) that Arabidopsis mutants defective in JA biosynthesis or perception are deficient in defense responses and are generally male sterile, while on the other hand, tomato mutants lacking JA biosynthesis or perception have deficient defense response but are male fertile (Howe et al., 1996; Li et al., 2001). In addition to that, recent studies have also demonstrated that ET and JA mediate the activation of various defense responses and confers resistance to certain pathogens. Similarly, in Arabidopsis, a MAP kinase named MPK4 gets activated within 2
5 minutes after wounding (Ichimura et al., 2000). A rapid increase in the concentration of JA was observed in roots of citrus plants just after salt stress imposition, reaching maximum levels of 6 hours after the onset of stress. It was found that treatment of stressed plants with methyl jasmonate (MeJA) before chilling rather than during or after stress imposition greatly improves the survival ratio of chilled rice seedlings (Lee et al., 1997). The first step of the synthesis of JA occurs in the membranes of chloroplasts, where a phospholipase releases α-linolenic acid (C18:3) and hexadecatrienoic acid (C16:3) from membrane phospholipids (Ishiguro et al., 2001; Hyun et al., 2008). In plants, its synthesis occurs primarily from the C18:3 precursors through the octadecanoid pathway (Farmer and Ryan 1992; Mueller et al., 1993). The second step constitutes oxidation of aLA by the action of a chloroplastic 13-lipoxygenase (13-LOX) generating the 13-hydroperoxy derivative of linolenic acid (13-HPOT). Chloroplastic 13-lipoxygenase oxidizes αLA which later forms the 13-hydroperoxy derivative of linolenic acid (Bannenberg et al., 2009).

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The Arabidopsis genome includes six genes’ encoding for lipoxygenases. Three of such genes are LOX2, LOX3, and LOX4 which regulate JA production (Santino et al., 2013; Caldelari et al., 2011). The next steps of JA synthesis occur in the peroxisome. JA synthesis proceeds with three rounds of β-oxidation which shortens the carbon side chain from the precursor molecule (Miersch and Wasternack 2000). The β-oxidation starts with the activation of OPC:8 by esterification to OPC:8-CoA (Baker et al., 2006; Koo and Howe 2007). Three different enzymes are involved in the central steps of β-oxidation which are arranged sequentially: (1) an acyl CoA oxidase (ACX) as ACX1 and ACX5 are involved in the synthesis of OPC:6 (Schilmiller et al., 2007), (2) a multifunctional protein encoded by the gene ABNORMAL INFLORESCENCE MERISTEM 1 (AIM1) which is involved in the synthesis of OPC:4CoA, and (3) a 3-ketoacyl-CoA thiolase (KAT2) which catalyzes the formation of JA-CoA (Castillo and Leo´n, 2008). Once synthesized, the (3R, 7S)-JA is then released into the cytoplasm from peroxisome by an unknown mechanism. Following the JA perception after the external stimuli, the signal transduction process assembles on basic helix
loop
helix related transcription factors, including the multifunctional MYC2 (Santino et al., 2013). During stress, a cluster of proteins, JASMONATE-ZIM-DOMAIN (JAZ) repressors control the response of JA. These JAZ repressors interact with CORONATINE INSENSITIVE1, which actually represents a part of the Skp-Cullin-F-box complex included in the coreception of biologically active JA (Yan et al., 2007; Santino et al., 2013).

21.2.8 Salicylic acid Phenolics in general, function as plant growth regulators. A broad range of organisms, either prokaryotic or eukaryotic including plants produce SA, a small phenolic molecule that plays a key role in plant defense response. A significant progress has been made in understanding SA-mediated defense signaling networks and the functional analysis of a large number of genes involved in the biosynthesis and regulation of SA accumulation and its signal transduction has revealed distinct but interconnecting pathways that orchestrate the control of plant defense (Lu, 2009). In a thermogenic plant named Voodoo lily, SA is the natural trigger of heat production by activating alternative respiration, which volatilizes putrid-smelling compounds that attract insects and helps in pollination. The critical role of SA in disease resistance has been demonstrated in other plants, including Arabidopsis, cucumber, and potato (Metraux et al., 1990; Delaney et al., 1994; Halim et al., 2007). A study conducted under the hydroponic system on maize plants shows that exogenous SA applied to the growth solution 1 day before the cold treatment decreased the effects of low temperature stress. Young maize plants were shown to exhibit increased cold tolerance upon treatment with SA (Janda et al., 1999). The activity of SA is concentration dependent and it has been scientifically proven that a lower dose of SA favors an increase in NR protein and a higher quantity of SA reverses the effects. Subsequently in the model plant Arabidopsis, the effect of SA has been proposed to increase the rate of oxidative damage generated by NaCl and osmotic stresses, thus causing seedling lethality (Borsani et al., 2001). Earlier experiments on various transgenic plants in which the synthesis and metabolism of SA was

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genetically altered proved that the presence of SA is needed for the development of stress symptoms and hypersensitive-response-like cell death. Although SA is not considered to be the main component of the signal translocated from the site of infection, its accumulation in distant tissues is highly essential for the induction of systemic acquired resistance (SAR) (Vernooij et al., 1994). It is clearly reported that SA not only influences a number of physiological responses but also allows the plants to increase the expression of alternative oxidase (Rhoads and McIntosh, 1992), thus enhancing cyanide-resistant respirational processes. Further, SA is involved in the initiation of an alternative respiratory pathway through the regulation of a specific nuclear gene which encodes for the alternative oxidase protein in Sauromatum guttatum (Rhoads and McIntosh, 1991). In a study by Hopke et al. (1994), the enhancement in growth of shoots and roots of soybean plants in response to SA treatment was reported. Dhaliwal et al. (1997) proved that SA also increases the leaf area in sugarcane plants, which is coherent with the previous results in maize plants. The difference in the amount of SA has different impact on the plants. Obvious effects on yield of various crop species have been achieved following the exogenous application of SA and a sudden increase in yield and number of pods has been observed in mung bean (Singh and Kaur, 1980). It is a general consent that the plants treated with SA have better fruit set and crop productivity, and in that line, an experiment conducted on wheat seedlings soaked in the solution of SA resulted in the possession of significantly higher leaf number, increased biomass production, and nitrate reductase and carbonic anhydrase activities than untreated ones (Hayat et al., 2012). Before hormonal signaling, the proteins are posttranslationally modified and these modifications are very crucial for the signaling pathway. In the SA pathway, activity of NPR1 is predominant, identified as master transcriptional coregulator of SA-dependent gene (Fu and Dong, 2013). SA also induces a biphasic fluctuation in the cellular redox state that can be sensed by NPR1 which is then translocated to the nucleus. The homologs of NPR1
NPR3 and NPR4 are reported to be SA receptors (Fu et al., 2012; Wu et al., 2012). Both NPR3 and NPR4 differ in their binding affinity for SA and binding capacity to NPR1, so that SA levels determine when NPR1 is targeted for degradation. Only when the levels of SA are low does NPR4 interact with NPR1, which leads to its degradation, and in this way untimely transcriptional activation in absence of SA is prevented, whereas high levels of SA facilitate binding between NPR1 and NPR3, again leading to removal of NPR1 (Fu et al., 2012). A substantial body of evidence suggests that SA is a critical signaling molecule in the pathway(s) leading to local and systemic disease resistance, as well as expression of pathogenesis-related gene (PR) in the plants studied so far. Two most probable routes for the biosynthesis of SA in plants have been discovered, which primarily differs at the point of hydroxylation of the aromatic ring and has been immensely described. The first step begins with the conversion of phenylalanine into cinnamic acid (CA). CA can be either hydroxylated to form O-coumaric acid by the oxidation of the side chain or can be initially oxidized to give benzoic acid which is later on hydroxylated in the ortho-position. Few scientists have also devised a third method for the most obvious pathway of production of SA and it is to be synthesized from Shikimic acid through chorismic and isochorismic acid, which was originally studied in bacteria but has

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recently been shown to take place in the chloroplast of the plants also (Wildermuth et al., 2001). These results are concomitant with the earlier findings on SA produced inside the plants.

21.3 Regulatory mechanism of phytohormones To regulate the growth and developmental processes responding to various internal and external stimuli, plants possess an internal scheme (Wani et al., 2016). By their involvement in fundamental processing of plants, they are considered as key components that directly or indirectly regulate the whole mechanism. Under several environmental changing conditions, they promote plants for acclimatizing against the environment by arbitrating their growth, source/sink transitions, and nutrient allocation (Wani et al., 2016). The rejoinder of plants against strains caused by abiotic factors depends on various factors. Among them, phytohormones are considered the most important endogenous substances for controlling physiological and molecular responses, a critical requirement for plant survival as sessile organisms. Under stress conditions, plants possess several strategies to cope with that, including hormone synthesis that plays a crucial role in their adaptation. The hormones such as SA, JA, ET, GA, and others are involved in plant defense signaling pathways. Among others, SA activates defense-related genes by two ways: (1) by H2O2-mediated signal transduction pathway and (2) by directly affecting mechanisms of metal detoxification (Metwally et al., 2003). SA inhibits two major H2O2 scavenging enzymes catalase (CAT) and ascorbate peroxidase (APX) that cause a rise in its cellular concentration and subsequently, at lower concentration, H2O2 acts as the second messenger for triggering defense against metal stress. Heavy metal stress induces ET biosynthesis (Milone et al., 2003) that acts as an endogenous signal triggering the plant defense response. The essential components of photosynthesis process include photosystem II, the xanthophyll cycle, and nonphotochemical quenching processes that were highly influenced by ABA. By increasing the antioxidant compound and enzyme activity, the stress tolerance capacity increases in the presence of ABA (Shen et al., 2017). Several studies reported that under stress conditions, increased antioxidant enzymes, such as superoxide dismutase (SOD), CAT, and APX, were noticed by increasing H2O2 content when ABA was exogenously applied (Christmann et al., 2006; Shen et al., 2017). Especially, under water-deficit conditions, it plays a vital role for plants in providing the ability to generate a signal cascade from shoots to roots when there is a stressful condition around the roots, ultimately resulting in water-saving antitranspirant activity, notably stomatal closure and reduced leaf expansion (Wilkinson et al., 2012). Further, the countenance of numerous stress-responsive genes is regulated by ABA and it also helps in the synthesis of late embryogenesis abundant (LEA) proteins, dehydrins, and other protective proteins (Sreenivasulu et al., 2012). It also controls the processes involved in maintenance of turgidity of cell and synthesis of osmoprotectants, and also the antioxidant enzymes conferring desiccation tolerance (Chaves et al., 2003). Even though auxin attained a keen interest for the plant physiologist for their role and behavior, its biosynthesis, transport, and signaling pathways are still not very clear. It is one of the most versatile plant hormones whose biosynthesis, signaling, and transport

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apparatus in green algae is an evidence for its evolutionary role during plant adaptation against diverse environment. It is considered as an integral part in the plants to cope with salinity stress by increasing root-and-shoot growth, and this phenomenon enhanced when SA provided to the plant exogenously represent the cross talk amongst phytohormones critical to signal perception and mediation of stress response. It works at transcriptional level and expresses a large number of genes called primary auxin response genes and hence, are regarded as an influential constituent of defense response. CKs are a key regulator plant hormone, which regulate the growth and development of plants. Any alternation in endogenous level causes stress to plant itself and also indicates its involvement in mitigating the vigorous effect of abiotic stress in plants (wani et al., 2016). Applying CK exogenously evaluated its effect on several stresses, also its internal biosynthesis enhanced under the influence of a stressful environment (Pospı´sˇ ilova´, 2003). GAs occur in different forms in plants but only GA1 and GA4 are found to be active in higher plants. Their predominant role is to enhance the seed germination, leaf expansion, stem elongation, flower, and trichome initiation, flower and fruit development, etc. (Yamaguchi, 2008). In several literatures, its defensive role against abiotic stresses is found to be more highlighting (Colebrook et al., 2014; Wani et al., 2016). It has been found that GA interacts with other phytohormones in numerous developmental and stimulusresponse processes. Depending upon the signal factors, its involvement with ET showed both negative and positive response to the plants. ET is a gaseous hormone involved by itself in several phases of plant growth and development as well as in plant responses to biotic and abiotic stresses. In higher plants, one of the plant hormones, ET, synthesizes with response to stress factors that mitigates the symptoms and makes the plant survive under adverse conditions. At severe stress conditions, its endogenous level varies or gets affected in plants. Heat stress is mainly mitigated under the influence of ET. One of the major roles of ET was also reported as protection of photosynthesis mechanism under Cd stress inducing synthesis of sulfur mediated regulation of glutathione (GSH) and antioxidant system modulation in Brassica juncea (Masood et al., 2012). It has been proposed to function via modulation of gene expression which is considered as the effectors of ET signal (Klay et al., 2014). The multifunctional compound, cyclopentanone, derived from membrane fatty acids including methyl jasmonate (MeJA) and JA which are collectively called JAs is mainly involved in plant developmental processes and survival together with reproduction, flowering, fruiting, senescence, secondary metabolism, and direct and indirect defense responses (Seo et al., 2001). With respect to defensive role, it activates plant defensive role against pathogens as well as environmental stresses, including salinity, UV radiation, and drought (wani et al., 2016). It has been reported that in soybean seedlings, MeJA lessened the salinity stress symptoms (Yoon et al., 2009). Moreover, JA activates genes that might be involved in the signal transduction pathway for Cd and upregulates GSH-metabolic genes and potentially enhances synthesis of GSH. Its application also alleviates the heavy metal stress in plants by enhancing antioxidant system (Yan et al., 2013). Xiang and Oliver (1998) reported that JA treatment increased the synthesis of GSH which helps in protection of plants from heavy metal stress. Furthermore, at transcription level also, JA-induced tolerance was largely controlled by increasing mRNA level in Arabidopsis thaliana (Xiang and Oliver 1998).

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SA, a naturally occurring phenolic compound, is involved mainly in the regulation of pathogenesis-associated protein expression. It plays a vital role in the defense system of plants against abiotic stress conditions and regulates the metabolic processes normally (Rivas-San and Plasencia, 2011; Hara et al., 2012). The SA signaling involves at least two mechanisms, one requiring NONEXPRESSOR OF PR GENES1 (NPR1) and the second MAPK that is independent of NPR1 (Yuan and Lin, 2008). For example, in A. thaliana, 10 MAPKKKK, 80 MAPKKK, 10 MAPKK, and 23 MAPK are reported which form complex SA-signaling networks, and MAP kinases: MPK3, MPK4, and MPK6 are activated by various abiotic stresses and might be central elements of SA-reactive oxygen species (SA-ROS) signal transduction. As a potent signaling molecule in plants it is involved in eliciting specific responses to biotic and abiotic stresses. As reported by Zhang et al. (2015), Cd toxicity can be regulated by SA via regulating the antioxidant defense mechanisms inhabited by plants itself.

21.4 Phytohormone-mediated modulation in plant under certain abiotic stresses Along with the regulation of growth and development processes of plants, phytohormones are also involved in biotic and abiotic stress responses. Plant responses to abiotic stresses can be viewed as being orchestrated through a network that integrates signaling pathways characterized by the activations of stress related genes and the production of phytohormones (Fig. 21.1). Although plant response against abiotic stresses depends on

Signal perception

Activation of stress responsive genes Radiation Cold Production of phytohormones

Heat

Increased adaptation and tolerance to stress

Stress signal

Salinity

Metal Root elongation

Pollen production Abiotic stresses

Herbivory Metal stress

Reproduction Senescence

FIGURE 21.1

Schematic depiction of activations of stress related genes and the production of phytohormones with response to abiotic stresses in plants.

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various factors, phytohormones are considered the most significant endogenous substances which are responsible for modulating physiological and molecular responses. Various abiotic stresses are known to cause crop losses worldwide and among them, drought, salinity, heat, cold, flooding, and UV radiation are main factors. Here we have discussed the regulatory mechanism of different phytohormones on plants under exposure of abiotic stresses.

21.4.1 Heavy metal stress Extensive intervention of human activities in the environment leads to the creation of pollution by increased toxic and hazardous materials, which becomes a major challenge for the world. In the age of rapid industrialization, heavy metal pollution becomes very common in the environment. It severely poses impacts on the ecological system due to which every component gets affected. Heavy metal contamination is very common in those countries which are struggling for their development such as India. Majorly their sources are mining, smelters, coal burning power plant, and excessive use of phosphate fertilizers in agriculture (Groppa et al., 2012; Bashri et al., 2015). Water pollution due to heavy metal stress is very common, due to which significant decrease in crop yield becomes a major problem (Singh and Prasad, 2014) for filling the gap between food demand and supply. According to World Health Organization (2007) and Singh and Prasad (2014), an increase in its amount in the environment causes hazardous effects on human health via entry through food chain. According to their role, they are classified as essential (Fe, Mn, Cu, Zn, and Ni) and nonessential (Cd, Pb, As, Hg, and Cr) (Dabonne et al., 2010; Anjum et al., 2016, 2017). Aluminum is not considered as a heavy metal, but it has the potential to cause toxicity that becomes a serious concern regarding plant growth and development by inducing a number of metabolic alterations (Anjum et al., 2017; Shahzad et al., 2018) resulting in damage to cell organelles. Some heavy metals are causing toxicity by generating ROS (Singh et al., 2015, 2017) and binding with sulfhydryl groups (
SH) in proteins which eventually leads to inhibition in their function and disturbing enzymatic structures (Hall, 2002; Shahzad et al., 2018). Majorly, metals cause toxicity by generating ROS inside the cell, which disrupts the membranes and other macromolecules via peroxidation of lipids. To cope with this problem, plants pose a defensive mechanism by equipping enzymatic and nonenzymatic antioxidants to protect the plant by scavenging ROS (Kumar et al., 2015; Singh et al., 2015, 2017). Cadmium is a very toxic metal and can cause damage even in traces. It is easily taken up by plants and it affects diverse morphological, structural, biochemical, and physiological attributes (Anjum et al., 2016; Ekmekci et al., 2008; Xu et al., 2015; Singh and Prasad, 2015). Studies showed that Cd inhibits photosynthetic process by limiting the use of ATP and NADPH in the Calvin cycle (Vassilev and Yordanov, 1997; Singh et al., 2015). It further induces the production and formation of ROS causing severe damage to membranes through peroxidation that ultimately results in cell death (Cho and Seo, 2005; Khan et al., 2007). Jonak et al. (2004) reported in their study that Cd increased the level of MAP-kinase activity resulting in increased production of ROS. Milone et al. (2003) and Singh and Prasad (2015) revealed the decreased production of SOD enzyme by which enhanced ROS

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content was noticed. Copper (Cu) is one of the essential micronutrients which is required by plants in trace amounts that directly involve itself for the growth and metabolic processes. According to Halliwell and Gutteridge (1984) free radical production intensifies the oxidative damage in cells by generating free radicals and inhibiting metabolism. Aluminum (Al) disrupts the plant growth by inhibiting certain enzymatic activities like δ-aminolevulinic acid dehydratase (Anjum et al., 2016). It mainly causes toxicity in the acidic condition of soil resulting in disruption of root growth and its physiology (Singh et al., 2017). It interferes with cell division process in the tips of the root, hinders the DNA replication process by enhancing the rigidity of DNA strands, reduces respiration in roots, disturbs the enzymatic activity, and nutrient balance (Vitorello et al., 2005; Singh et al., 2017). Zobel et al. (2007) observed reduced root growth and increased root diameter under Al stress. Detrimental effects of Al in different plant species such as wheat (Hossain et al., 2005), barley (Guo et al., 2004), green gram (Panda et al., 2003), and triticale (Liu et al., 2008) have been reported through lipid peroxidation. Nickel (Ni) is an integral part of several enzymes such as urease; its deficiency disrupts the nitrogen assimilation in several pant species. It also shows negative effect on several metabolic processes such as nutrient absorption, photosynthesis, and evapo-transpiration (Rahman et al., 2005). Its excess accumulation in cell is responsible for generation of ROS resulting in membrane damage by lipid peroxidation (Gajewska and Skłodowska, 2008). Several reports have clarified that plant hormones, such as ABA, JA, SA, IAA, CKs, and ¨ zdemir et al., BR, are involved in the regulatory process for antioxidant production (O 2004; Sharma and Bhardwaj, 2007; Sharma et al., 2011; Ramakrishna and Rao, 2012; Kapoor et al., 2014). IAA is one of the most diversified phytohormones and plays a vital role in plant growth and development under normal as well stress conditions. It is regarded as an influential constituent of defense responses via regulation of numerous genes and mediation of cross talk between different stresses. ABA is a stress hormone that plays a critical role in resolving the problems of plants under several stress conditions. In plants, an increase in ABA level implies the resistivity against stress conditions including metal, drought, and cold (Christmann et al., 2006). In several studies, it has been reported that exogenously supplied ABA results in the synthesis of H2O2 which in turn enhances the expression of gene encoding antioxidant enzymes, leading to increased activity of enzymes (Bellaire et al., 2000; Jiang and Zhang, 2001) which ultimately increases the stress tolerance of plants. This was justified by Janowiak et al. (2002) and Sripinyowanich et al. (2013) that pretreatment of ABA increases the resistivity of corn (Zea mays) to temperature and water stress, also improved the salt resistance of rice and alleviated the toxic effect of Cd on rice. Although it has been reported that almost every phytohormone is involved in plant defense responses against various biotic and abiotic stresses, the work with BRs, JA, SA and ET have emerging roles and presented new perspectives on stress tolerance studies. Being well characterized and studied role of SA in pathogen resistance, the exogenous application of SA could also provide protection against several types of abiotic stresses including heavy metal. The treatment of SA to plants might have an acclimation-like effect, causing enhanced tolerance towards metal stress predominantly by the adjustment of metabolic processes such as enhanced antioxidative capacity. In pea seedlings, Cd toxicity caused decline in growth due to the inhibited photosynthetic process and enhanced

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oxidative damage while SA pretreatment alleviated damaging consequences (Popova et al., 2009). In addition to this, BRs were also reported to reduce the adverse effects of Cd stress in plants. The role of two active forms of BRs such as 28-homobrassinolide (28-HBL) or 24-epibrassinosteroid (24-EBL) in Cd-exposed plant species has been extensively reported by Anuradha and Rao (2009) and Vazquez et al. (2013). These authors have evidently proved that 28-HBL or 24-EBL mediated improved plant growth, photosynthesis, and metabolism mainly due to enhanced level of antioxidants. These defending enzymes in plant cell such as SOD, CAT, ascorbate peroxidase (APOX), and peroxidase (POD) were also improved, suggesting that their activities were regulated with EBL treatment (Kanwar et al., 2013). An interaction between the plant hormones auxin, BRs, ET, ABA, SA, and JA under heavy metal exposure is shown in Fig. 21.2. Further, Anuradha and Rao (2007) unrevealed that in Raphanus sativus L. seedlings, 24-epibrassinolide ameliorated the Cd toxicity by enhancing free proline and also by increasing the activities of enzymes such as SOD, CAT, APX, and GPOD. 24-Epibrassinolide also reduces the detrimental effects of Cu in plants as reported by Fariduddin et al. (2013) by improving morphological attributes and biomass accumulation (Fariduddin et al., 2009). They further confirmed that EBL also minimizes the ROS content by increasing the enzymatic activities which directly influence the growth of the plant (Fariduddin et al., 2013). Under aluminum stress also, EBL plays a significant role in enhancing the defensive mechanism in plants by increasing the antioxidant enzymes which alleviate the toxicity and increase the plant’s metabolic activity resulting in increased growth and biomass (Ali et al., 2008). Abdullahi et al. (2003) also found the similar effect of EBL on mung bean (Vigna radiata) when subjected to Al stress. Madhan et al. (2014) reported the ameliorative role of EBL on pigeon pea (Cajanus cajan L.) under Al stress. Likewise to Al stress amelioration, Ni stress also ameliorated in the presence of EBL. Kanwar et al. (2013) reported the potentiality of EBL in B. juncea under Ni stress and reduction in Ni uptake by plant.

21.4.2 Water stress Water stress or drought is one of the consequences of irregular rainfall that becomes a constraint to the plants, both wild species as well as crop plants. Moreover, most of the soils have variability in wet capacity resulting in a heterogeneous moisture profile following precipitation and irrigation. Plants are naturally distributed in varied conditions of water; at scarce place, they possess modified morphology and anatomy for water conversion. This kind of resistance is basically for drought resistance. On the other hand, mesophytic plants have differently adapted to tolerance towards water stress. Mechanism of such tolerance involves a variation in working network and sequential events leading to alleviation of potential stress-induced cellular injuries depending on the plant species that have evolved through environmental changes (Kar, 2011). Responses of plants against water stress may be considered at the whole plant level as an integrated tissue system while some of the responses occur at the cellular level. Closing of stomata is one of the survival strategies of plants in water stress condition that results from some indirect biochemical and molecular changes in the guard cell itself, but this event is ultimately induced by the signal transduced by the cell. Seeds differently respond to the water stress.

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Heavy metals Induces Sensors

ROS generation

NO

an Signal tr sduction ACS 1,2,6 ACO 4,5

Cu Cd

Root elongation

ROS generation

BR

Auxin

V As SA/JA

ABA

Ethlylene ETHYLENE SIGNALING

Cd CTRI

H2O2

SOD POD CAT

POD CAT H2O2

Pb Pb

Pb Pb

NO ICa

EIN2 Pb Pb Pb Pb Pb

Channels S-type anion Channels

AtPD R12

Pb Pb Pb Pb Pb

Flavenoids phytochelatins phytoalexins

Response

FIGURE 21.2 Diagrammatic representation showing some interactions between the plant hormones and heavy metal exposure. Cd treatments increased activity of auxin resulting in increase in activity of POD and CAT which ultimately blocks the increase in H2O2 content. Auxin in presence of Cu regulates the synthesis of NO which ultimately blocks the stem elongation by minimizing the auxin transport. Under As and V stress, trigger the expression of certain genes associated with ABA signaling and biosynthesis. BRs induce SOD, CAT, and POD activities, protecting plants against heavy metal toxicity. ACS and ACO expression leads to higher production of ethylene. Lead treatment increased the transcript levels of EIN2 in Arabidopsis seedlings under heavy metal exposure. It has been suggested that EIN2 regulates AtPDR12, an ABC membrane-transporter that excludes Pb and Pb-containing toxic compounds from the cytoplasm. Arrows and T-bars represent positive and negative regulation, respectively. Green arrows (gray in print version) indicate increased levels. ABC, ATP-binding cassette; ACO, ACC oxidase; ACS, ACC synthetase; As, arsenic; BRs, brassinosteroids; CAT, catalase; Cd, cadmium; Cu, copper; JA, jasmonic acid; NO, nitric oxide; Pb, lead; POD, peroxidase; SA, salicylic acid; SOD, superoxide; V, vanadium.

Seed germination declines when there is water scarcity while proteolysis in cotyledons is retarded by water stress (Kar, 2011). Noctor et al. (2002) reported that drought stress is resulting in increased production of ROS. To resolve the ROS problem, plants possess mitigating strategies such as production of defensive enzymes as well as some metabolites as a scavenger of ROS, such as SOD, CAT, glutathione-S-transferase, and ascorbate.

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Among the phytohormones, ABA is considered as the most important hormone for playing a role in signaling for tolerance against drought. Its main action against drought is stomata closing. Recent studies proved that this mechanism occurs by the action of ROS particularly H2O2, which is synthesized by plasma membrane-bound NADPH oxidase (Kwak et al., 2003). Another hormone ET is associated with the drought stress, which increases under stress and is directly influenced by ROS content. ET has also been implicated, in some plants, for stomata closure and ETR1, one of the ET receptors, is involved in H2O2 sensing resulting in stomata closing (Desikan et al., 2005).

21.4.3 Salt stress Salinity is one of the major environmental limitations to crop production, which is considered as a worldwide problem. Seven percent of the land’s surface and 5% of cultivated lands are affected by salinity, and it is an important factor that can limit the growth and productivity of plants. The harmful effect caused by salinity is mainly due to the ionic and osmotic imbalance (Magome et al., 2008). According to Parida and Das (2005), salt stress affects some basic metabolic processes in plants such as photosynthesis, lipid metabolism, and protein synthesis. Decrease in photosynthetic rates under salt stress is mainly due to the reduction in photosynthetic pigments (Dubey, 2005), as well as limitations in photosynthetic electron transport and partial stomatal closure (Zhang et al., 2010). In addition, the production of ROS, including superoxide radical (O22), hydroxyl radical (•OH), singlet oxygen (1O2), and hydrogen peroxide (H2O2), are the characteristics of biochemical changes during salt stress. High salt concentration (in terms of Na1) in particular, deposited in the soil, possesses alteration in basic texture of the soil resulting in decreased soil porosity and consequently, reduced soil aeration and water conductance (Mahajan and Tuteja, 2005). In response to this damage, various genes are upregulated, which can mitigate the damage and lead to adjustment of the cellular environment and plant tolerance. A study governed with 24-epiBL treatment has been shown to significantly increase fresh ¨ zdemir et al., 2004). weight and dry weight of rice seedling shoots under salinity stress (O Similarly, growth promotion in Chinese cabbage mesophyll protoplasts by 24-epiBL was associated with increased amounts of soluble proteins. In the study, salt stress growth characteristics of common bean seedlings under salinity stress were markedly improved by applying GAs. GA is also reported as the growth promoter of salinity stress in wheat, maize, and tomato (Kaya et al., 2006). Salt stress was strong enough to inhibit plant growth due to reduction in gibberellin production (Kaya et al., 2006). Growth can be increased through GA3 by improving plant growth and chlorophyll synthesis. Gibberellins appear to play a key role against oxidative stress by decreasing accumulation of ROS resulting in the prevention of lipid peroxidation, which were induced by salinity. These alleviating effects of GA3 were highly correlated with the increasing activities of antioxidant enzymes.

21.4.4 Ultraviolet-B stress UV stress is one of the highly targeting stresses for the plants. The level of UV radiations in the environment is increasing day by day and the plants, which use direct sunlight

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21. Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects

for photosynthesis, are unable to avoid UV radiations which impart adverse effects on physiological processes. Stress effects occur mainly at high doses of UV-B in nonacclimated plants, while low levels of UV-B can induce true photo-morphogenic effect in the plant without any signs of stress (Jenkins, 2009; Jansen and Bornman, 2012). For more than 20 years, because of anthropogenic activity, ozone destroying chlorine and bromine halocarbon has led to a steady increase in the concentration of these compounds in the atmosphere and has resulted in the progressive destruction of the ozone layer. A minor increase in UV-B in the atmosphere leads to significant biological damage not only in plants but also human beings are also affected by the same. Studies have shown that under UV-B stress conditions, reduction in RuBisCO levels is the primary cause for the decline in photosynthetic rate (Allen et al., 1997). At transcriptional level, transcripts encoding small and large subunits RbcS and rbcL decreased respectively (Rao et al., 1995). Similar results were also observed with respect to expression of Lhcb, encoding the light harvesting complex and psbA, encoding the D1 polypeptide of PS II. Several studies have shown that UV-B exposure leads to oxidative stress in plants. This can be proved experimentally by using spin trapping EPR spectroscopy, which evidences the ROS generation within thylakoid membranes isolated from UV-B treated plants. Therefore the mechanisms that may protect the plants from the harmful effects of UV exposure or ozone stress are of particular concern. The application of phytohormones is nowadays an emerging tool for minimizing the harmful effect of UV damage in plants. As studies revealed, SA has been frequently associated with UV-B regulated growth merely based on the UV-B-mediated changes in the expression of auxin-related genes in seedlings and mature leaves. It has been previously reported that SA is accumulated regularly when the plant is exposed to UV-B stress (Yalpani et al., 1991). In A. thaliana, the role of SA was best demonstrated in counteracting the damaging effects of ozone, where NahG mutants deficient in SA biosynthesis were more sensitive to the deteriorating effects of ozone (Sharma et al., 1996). Accumulation of SA in tobacco plants was also reported and this increased accumulation of SA was probably due to higher activity of the enzyme BAZ-hydroxylase, which is involved in SA biosynthesis. The exogenous application of SA alleviated the damaging effects induced by UV-B radiation exposure in Kentucky bluegrass and tall fescue sod (Ervin et al., 2004). Studies revealed that the activities of antioxidant enzymes CAT and SOD were greatly reduced by UV-B exposure. The anthocyanin and α-tocopherol contents also increased in the UV-B stressed plants treated with SA. Thus it can be concluded that the concentration of different plant hormones appear to be important in regulating stress responses. The phytohormone-mediated physio-biochemical alterations involved in mediating abiotic stress tolerance are summarized in Table 21.2.

21.5 Future perspective In this chapter, some of the most significant details regarding the production of plant hormones, their signaling pathways under different abiotic stress conditions were reviewed. Regarding growth augmentation and productivity of plants grown under influence of different phytohormones as compared to untreated plants, there are well-known

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21.5 Future perspective

TABLE 21.2 Phytohormones-induced physiological and biochemical changes to alleviate toxicity in plants grown under abiotic stresses. Types of stress

Studied plant

Mitigation by phytohormones

1.

Salinity

Wheat

2.

Salinity

Zea mays

3.

None

4.

Effect

References

Auxin, gibberellin, zeatin, and ethephon

Seed dormancy was alleviated by the application of different phytohormones in wheat plant

Egamberdieva (2009)

Auxin

Activities of different types of enzymatic antioxidants were increased in saline condition. IAA significantly reduced sodium ion concentration and improved K1, Ca21, and P levels. Growth promotion was found to be directly associated with increase in photosynthetic pigment content and reduced membrane permeability

Kaya et al. (2013)

Pinus Auxins yunnanensis

Both the phytohormones were effectively promoting the growth of plant resulting in increase in biomass. Increment in biomass of needle and root and shoot were noticed when both the hormones were combined together

Xu et al. (2012)

Salt

Zea mays L. Auxin

Salt stress effectively reduced the growth and photosynthesis. However, this reduction was alleviated by the application of IAA. Simultaneously, Na1 accumulation was reduced in shoot and roots

Khalid et al. (2013)

5.

Cadmium

Solanum melongena

Kinetin

Reduces Cd uptake and transport, increases growth, and photosynthesis

Singh and Prasad (2014)

6.

Cadmium

Trigonella sp.

Auxin

Improves photosynthetic efficiency and antioxidant potential

Bashri et al. (2015)

7.

Cadmium

Pisum sativum

Salicylic acid

Enhances growth, pigment contents, and photosynthesis

Popova et al. (2009) (Continued)

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21. Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects

TABLE 21.2 (Continued) Types of stress

Studied plant

Mitigation by phytohormones

Effect

References

8.

Mercury

Luffa cylindrica

Auxin

Reduces diameter of Khan and internode and inhibition in Chaudhry cortical, sclerenchyma, (2006) cambial, and pith region were noticed under mercury stress. IAA alone enhances growth of cambium and cortical region as well as large xylem vessel. IAA in combination with HgCl2 decreases the harmful effect in all the parameters

9.

Copper

Helianthus annuus L.

Auxin, Gibberellin

The photosynthetic pigment Ouzounidou content decreases and Ilias (2005) significantly resulting in decrease in photosynthesis. Transpiration rates were also decreased. Applying both the phytohormones significantly alleviates the damaging effect of mercury in all the parameters

10. None

Allium cepa L.

Auxin, salicylic acid

Application of both the Amin et al. hormones led to increase in (2007) vegetative growth. Increase in pigment content was also noticed. Increase in total soluble sugar, total free amino acids, total phenol, and total indoles were also noticed in the presence of SA specifically

11. Zn

Raphanus sativus L.

24-EBL

Enhancement in the level of Ramakrishna membrane lipid peroxidation, and Rao (2012) protein oxidation, contents of hydrogen peroxide, and hydroxyl radical, the production rate of superoxide radicals indicate the occurrence of oxidative stress. EBR minimizes the extent of oxidative stress by enhancing the activity of defensive enzymes superoxide dismutase, guaiacol peroxidase, glutathione peroxidase, and peroxidase in radish seedlings (Continued)

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21.5 Future perspective

TABLE 21.2

(Continued) Studied plant

Mitigation by phytohormones

12. Chilling stress

Cucumis sativus L.

28-HBL

The most evident effect of Fariduddin chilling treatment to the et al. (2011) plants was the reduction in growth, chlorophyll content due to which the net photosynthetic rate was also decreased. The activity of PS II, nitrate reductase, and carbonic anhydrase were also decreased. The protective role of HBL was focused in improved growth, water relations, photosynthesis, and maximum quantum yield of PS II in presence or absence of chilling stress

13. UV radiation (UV-A, UV-B, UV-C)

Glycine max L.

Epibrassinosteroid

Decrease in chlorophyll a and Enteshari et al. b, and carotenoid content (2006) were examined in the presence of UV-B and UV-C. Epibrassinosteroid minimizes the decrease in pigment content. Anthocyanin, flavonoids, and UV absorbing compounds in plants which are treated with UV-B/UV-C and epibrassinosteroid were found to be increased

14. Draught stress

Glycine max L.

Brassinolide

Mainly, decrease in biomass Zhang et al. accumulation and seed yield (2008) was noticed. While both factors were enhanced by applying BR to the plants. The maximum quantum yield of PS II, activity of RuBisCO, and the leaf water potential were also increased in draught stressed plant

15. Draught stress

Brassica juncea L.

28-HBL

Plant grown in draught condition when subjected to HBL showed increase in growth and photosynthesis. Activity of antioxidant enzymes, that is, SOD, POD, and CAT as well as proline content were found to increased

Types of stress

Effect

EBL, Epibrassinolid; HBL, homobrassinolide.

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References

Fariduddin et al. (2009)

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21. Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects

validations available. But there are still gaps in the knowledge whether phytohormones could compensate for the upregulation of defense-related genes or signaling mechanism against stress and what are the mechanisms behind it. In view of the importance of phytohormones, there is a tremendous scope for further research focused on the sites, pathways, and enzymology of their biosynthesis, developmental, and physiological processes under stress conditions. Clarification of such details may result in the production of transgenic plants, which are more tolerant under stress.

References Abbas, S., Latif, H.H., Elsherbiny, E.A., 2013. Effect of 24-epibrassinolide on the physiological and genetic changes on two varieties of pepper under salt stress conditions. Pak. Bot. 45, 1273
1284. Abdullahi, B.A., Gu, X.G., Gan, Q.L., Yang, Y.H., 2003. Brassinolide amelioration of aluminium toxicity in mung bean seedling growth. J. Plant Nutr. 26, 1725
1734. Ali, B., Hasan, S.A., Hayat, S., Hayat, Q., Yadav, S., Fariduddin, Q., et al., 2008. A role for brassinosteroids in the amelioration of aluminium stress through antioxidant system in mung bean (Vigna radiata L. Wilczek). Environ. Exp. Bot. 62, 153
159. Allen, D.J., McKee, I.F., Farage, P.K., Baker, N.R., 1997. Analysis of the limitation to CO2 assimilation on the exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ. 20, 633
640. Amin, A.A., Sh, E.L., Rashad, M., EL-Abagy, H.M.H., 2007. Physiological effect of indole-3-butyric acid and salicylic acid on growth, yield and chemical constituents of onion plants. J. App. Sci. Res. 3 (11), 1554
1563. Anjum, S.A., Tanveer, M., Hussain, S., Shahzad, B., Ashraf, U., Fahad, S., et al., 2016. Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environ. Sci. Pollut. Res. Int. 23, 11864
11875. Anjum, S.A., Tanveer, M., Hussain, S., Ashraf, U., Khan, I., 2017. Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress. Water Air Soil Pollut. 228, 13. Anuradha, S., Rao, S.S.R., 2007. Effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. Plant Soil Environ. 53, 465
472. Anuradha, S., Rao, S.S.R., 2009. Effect of 24-epibrassinolide on the photosynthetic activity of radish plants under cadmium stress. Photosynthetica 47, 317
320. Bajguz, A., 2010. An enhancing effect of exogenous brassinolide on the growth and antioxidant activity in Chlorella vulgaris cultures under heavy metals stress. Environ. Exp. Bot. 68, 175
179. Baker, A., Graham, I.A., Holdsworth, M., Smith, S.M., Theodoulou, F.L., 2006. Chewing the fat: beta-oxidation in signalling and development. Trends Plant Sci. 11, 124
132. Bannenberg, G., Martı´nez, M., Hamberg, M., Castresana, C., 2009. Diversity of the enzymatic activity in the lipoxygenase gene family of Arabidopsis thaliana. Lipids 44, 85
89. Bashri, G., Singh, S., Singh, A., Prasad, S.M., 2015. Changes in physiological attributes and biochemical marker responses in vegetable crops grown under cadmium stress: a comparative study. Plant Archives 15, 163
170. Bellaire, B.A., Carmody, J., Braud, J., Gossett, D.R., Banks, S.W., Cranlucas, M., et al., 2000. Involvement of abscisic acid-dependent and -independent pathways in the upregulation of antioxidant enzyme activity during NaCl stress in cotton callus tissue. Free Radic. Res. 33, 531
545. Bennett, M.J., Marchant, A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A., et al., 1996. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948
950. Borsani, O., Valpuesta, V., Botella, M.A., 2001. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol. 126, 1024
1030. Boyer, J.S., 1982. Plant productivity and environment. Science 218, 443
448. Caldelari, D., Wang, G., Farmer, E.E., Dong, X., 2011. Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Mol. Biol. 75, 25
33. Campos, M.L., Kang, J.H., Howe, G.A., 2014. Jasmonate-triggered plant immunity. J. Chem. Ecol. 40, 657
675.

Plant Life under Changing Environment

References

569

Castillo, M.C., Leo´n, J., 2008. Expression of the beta-oxidation gene 3-ketoacyl-CoA thiolase 2 (KAT2) is required for the timely onset of natural and dark-induced leaf senescence in Arabidopsis. J. Exp. Bot. 59, 2171
2179. Cho, U.H., Seo, N.H., 2005. Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci. 168, 113
120. Chory, J., Nagpal, P., Peto, C.A., 1991. Phenotypic and genetic analysis of DET2 a new mutant that affects lightregulated seedling development in Arabidopsis. Plant Cell. 3, 445
460. Christmann, A., Moes, D., Himmelbach, A., Yang, Y., Tang, Y., Grill, E., 2006. Integration of abscisic acid signalling into plant responses. Plant Biol. 8, 314
325. Chaves, M.M., Maroco, J.P., Pereira, J.S., 2003. Understanding plant responses to drought-from genes to the whole plant. Funct. Plant Biol. 30, 239
264. Coakley, S.M., Scherm, H., Chakraborty, S., 1999. Climate change and plant disease management. Annu. Rev. Phytopathol. 37, 399
426. Cohen, J.D., Slovin, J.P., Hendrickson, A.M., 2003. Two genetically discrete pathways convert tryptophan to auxin: more redundancy in auxin biosynthesis. Trends Plant Sci. 8, 197
199. Colebrook, E.H., Thomas, S.G., Phillips, A.L., Hedden, P., 2014. The role of gibberellin signaling in plant responses to abiotic stress. J. Exp. Biol. 217, 67
75. Constabel, C.P., Bergey, D.R., Ryan, C.A., 1995. Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 92, 407
411. Dabonne, S., Koffi, B., Kouadio, E., Koffi, A., Due, E., Kouame, L., 2010. Traditional utensils: potential sources of poisoning by heavy metals. Br. J. Pharm. Toxicol. 1, 90
92. Debez, A., Chaibi, W., Bouzid, S., 2001. Effect du NaCl et de regulateurs de croissance sur la germination d’ Atriplex halimus L. Cah. Agric. 10, 135
138. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., et al., 1994. A central role of salicylic acid in plant disease resistance. Science 266, 1247
1250. Desikan, R., Hancock, J.T., Bright, J., Harrison, J., Weir, I., Hooley, R., et al., 2005. A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol. 137, 831
834. Dhaliwal, R.K., Malik, C.P., Gosal, S.S., Dhaliwal, L.S., 1997. Studies on hardening of micropropagated sugarcane (Saccharum officinarum L.) plantlet. II. Leaf parameters and biochemical estimations. Ann. Biol. Ludhiana 13, 15
20. Dharmasiri, N., Dharmasiri, S., Estelle, M., 2005a. The F-box protein TIR1 is an auxin receptor. Nature 435, 441
445. Dharmasiri, N., Dharmasiri, S., Weijers, D., Lechner, E., Yamada, M., Hobbie, L., et al., 2005b. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9, 109
119. Dievart, A., Clark, S.E., 2003. Using mutant alleles to determine the structure and function of leucine-rich repeat receptor-like kinases. Curr. Opin. Plant Biol. 6, 507
516. Dill, A., Thomas, S.G., Hu, J., Steber, C.M., Sun, T., 2004. The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16, 1392
1405. Doares, S.H., Narvaez-Vasquez, J., Conconi, A., Ryan, C.A., 1995. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108, 1741
1746. Dubey, R.S., 2005. Photosynthesis in plants under stressful conditions. Handbook of Photosynthesis. CRC Press, Boca Raton, FL, pp. 479
497. Egamberdieva, D., 2009. Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol. Plant. 31, 861
864. Ekmekci, Y., Tanyolac, D., Ayhan, B., 2008. Effect of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J. Plant Physiol. 165, 600
611. Enteshari, S.H., Kalantari, K.H., Ghorbanli, M., 2006. The effect of epibrassinosteroid and different bands of ultraviolet radiation on the pigments content in Glycine max L. Pak. J. Biol. Sci. 9 (2), 231. Ervin, E.H., Zhang, X.Z., Fike, J.H., 2004. Ultraviolet-B radiation damage on Kentucky Bluegrass II: hormone supplement effects. Hortscience 39, 1471
1474. Fahad, S., Hussain, S., Matloob, A., Khan, F.A., Khaliq, A., Saud, S., et al., 2015. Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul. 75, 391
404. Fariduddin, Q., Yusuf, M., Hayat, S., Ahmad, A., 2009. Effect of 28-homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to different levels of copper. Environ. Exp. Bot. 66, 418
424.

Plant Life under Changing Environment

570

21. Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects

Fariduddin, Q., Yusuf, M., Chalkoo, S., Hayat, S., Ahmad, A., 2011. 28-Homobrassinolide improves growth and photosynthesis in Cucumis sativus L. through an enhanced antioxidant system in the presence of chilling stress. Photosynthetica 49 (1), 55
64. Fariduddin, Q., Khalil, R.R., Mir, B.A., Yusuf, M., Ahmad, A., 2013. 24-Epibrassinolide regulates photosynthesis, antioxidant enzyme activities and proline content of Cucumis sativus under salt and/or copper stress. Environ. Monit. Assess. 185, 7845
7856. Farmer, E.E., Ryan, C.A., 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of woundinducible proteinase inhibitors. Plant Cell 4 (2), 129
134. Feys, B., Benedetti, C.E., Penfold, C.N., Turner, J.G., 1994. Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6, 751
759. Finkelstein, R.R., Gampala, S.S.L., Rock, C.D., 2002. Abscisic acid signaling in seeds and seedlings. Plant Cell 14, 15
45. Friml, J., Benkova, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., et al., 2002. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661
673. Fu, Z.Q., Dong, X., 2013. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64, 839
863. Fu, Z.Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486, 228
232. Gajewska, E., Skłodowska, M., 2008. Differential biochemical responses of wheat shoots and roots to nickel stress: antioxidative reactions and proline accumulation. Plant Growth Regul. 54, 179
188. Ga¨lweiler, L., Guan, C., Mu¨ller, A., Wisman, E., Mendgen, K., Yephremov, A., et al., 1998. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226
2230. Gray, W.M., Kepinski, S., Rouse, D., Leyser, O., Estelle, M., 2001. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271
276. Grazzini, E., Guillon, G., Mouillac, B., Zingg, H.H., 1998. Inhibition of oxytocin receptor function by direct binding of progesterone. Nature 392, 509
512. Groppa, M.D., Ianuzzo, M.P., Rosales, E.P., Va´zquez, S.C., Benavides, M.P., 2012. Cadmium modulates NADPH oxidase activity and expression in sunflower leaves. Biol. Plant 56, 167
171. Guilfoyle, T., Hagen, G., Ulmasov, T., Murfett, J., 1998. How does auxin turn on genes? Plant Physiol. 118, 341
347. Guo, T., Zhang, G., Zhou, M., Wu, F., Chen, J., 2004. Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258, 241
248. Hagen, G., Guilfoyle, T., 2002. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49, 373
385. Halim, V.A., Eschen-Lippold, L., Altmann, S., Birschwilks, M., Scheel, D., 2007. Salicylic acid is important for basal defense of Solanum tuberosum against Phytophthora infestans. Mol. Plant Microbe Interact. 20, 1346
1352. Hall, J.L., 2002. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 53, 1
11. Halliwell, B., Gutteridge, J.M., 1984. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem. J. 219, 1
14. Hamilton, A.J., Bouzayen, M., Grierson, D., 1991. Identification of a tomato gene for the ethylene-forming enzyme by expression in yeast. Proc. Natl. Acad. Sci. U.S.A. 88, 7434
7437. Hara, M., Furukawa, J., Sato, A., Mizoguchi, T., Miura, K., 2012. Abiotic stress and role of salicylic acid in plants, Abiotic Stress Responses in Plants, 2012. Springer, New York, pp. 235
251. Hayat, Q., Hayat, S., Irfan, M., Ahmad, A., 2012. Effect of exogenous salicylic acid under changing environment: a review. Environ. Exp. Bot 68, 14
25. He, Z., Wang, Z.Y., Li, J., Zhu, Q., Lamb, C., Ronald, P., et al., 2003. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288, 2360
2363. Himmelbach, A., Yang, Y., 2003. Grill E. Relay and control of abscisic acid signaling. Curr. Opin. Plant Biol. 6, 470
479. Hopke, J., Donath, J., Blechert, S., Boland, W., 1994. Herbivore induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a b-glucosidase and jasmonic acid. FEBS Lett. 352, 146
150.

Plant Life under Changing Environment

References

571

Hossain, M.A., Hossain, A.K.M.Z., Kihara, T., Koyama, H., Hara, T., 2005. Aluminum-induced lipid peroxidation and lignin deposition are associated with an increase in H2O2 generation in wheat seedlings. Soil Sci. Plant Nutr. 51, 223
230. Howe, G.A., Lightner, J., Browse, J., Ryan, C.A., 1996. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8, 2067
2077. Lu, H., 2009. Dissection of salicylic acid-mediated defense signaling networks. Plant Signal. Behav 4 (8), 713
717. Hwang, I., Sheen, J., 2001. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383
389. Hyun, Y., Choi, S., Hwang, H.J., Yu, J., Nam, S.J., Ko, J., et al., 2008. Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis. Dev. Cell 14, 183
192. Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T., Shinozaki, K., 2000. Various abiotic stresses vapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant 24, 655
665. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., et al., 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409, 1060
1063. Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I., Okada, K., 2001. The defective in anther dehiscience gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13, 2191
2209. Jackson, M., 1997. Hormones from roots as signals for the shoots of stressed plants. Elsevier Trends 2, 22
28. Janda, T., Szalai, G., Tari, I., Pa´ldi, E., 1999. Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208 (2), 175
180. Janowiak, F., Maas, B., Dorffling, K., 2002. Importance of abscisic acid for chilling tolerance of maize seedlings. J. Plant Physiol. 159, 635
643. Jansen, M., Bornman, J.F., 2012. UV-B radiation: from generic stressor to specific regulator. Physiol. Plant. 145, 501
504. Jenkins, G.I., 2009. Signal transduction in responses to UV-B radiation. Ann. Rev. Plant Biol. 60, 407
431. Jiang, M., Zhang, J., 2001. Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol. 42, 1265
1273. Jonak, C., Nakagami, H., Hirt, H., 2004. Heavy metal stress activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol. 136, 3276
3283. Kakimoto, T., 1996. CKI1, a cystidine kinase homolog implicated in cytokinin signal transduction. Science 274, 982
985. Kang, N.Y., Cho, C., Kim, N.Y., Kim, J., 2012. Cytokinin receptor-dependent and receptor-independent path ways in the dehydration response of Arabidopsis thaliana. Plant Physiol. 169, 1382
1391. Kanwar, M.K., Bhardwaj, R., Chowdhary, S.P., Arora, P., Sharma, P., Kumar, S., 2013. Isolation and characterization of 24-Epibrassinolide from Brassica juncea L. and its effects on growth, Ni ion uptake, antioxidant defense of Brassica plants and in vitro cytotoxicity. Acta Physiol. Plant 35, 1351
1362. Kapoor, D., Kaur, S., Bhardwaj, R., 2014. Physiological and biochemical changes in Brassica juncea plants under Cd-induced stress. BioMed Res. Int. Available from: https://doi.org/10.1155/2014/726070. Kar, R.K., 2011. Plant response to water stress, role of reactive oxygen species. Plant Signal. Behav. 6, 1741
1745. Kaya, M.D., Okc¸u, G., Atak, M., C ¸ ikili, Y., Kolsarici, O., 2006. Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). Eur. J. Agron. 24, 291
295. Kaya, C., Ashraf, M., Dikilitas, M., Tuna, A.L., 2013. Alleviation of salt stress-induced adverse effects on maize plants by exogenous application of indoleacetic acid (IAA) and inorganic nutrients
a field trial. Aust. J. Crop Sci. 7, 249
254. Khalid, S., Parvaiz, M., Nawaz, M., Hussain, K., Arshad, A., Shawakat, S., et al., 2013. Effect of indole acetic acid (IAA) on morphological, biochemical and chemical attributes of two varieties of maize (Zea mays L.) Under Salt Stress. World Appl. Sci. J. 26 (9), 1150
1159. Khan, A.S., Chaudhry, N.Y., 2006. Auxins partially restore the cambial activity in Luffa cylindrica L. (Cucurbitaceace) under mercury stress. Int. J. Food, Agric. Environ. 4 (1), 276
281. Khan, N.A., Singh, S., Nazar, R., 2007. Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J. Agron. Crop Sci. 193, 435
444. Klay, I., Pirrello, J., Riahi, l, Bernadac, A., Cherif, A., Bouzayen, M., et al., 2014. Ethylene response factor Sl-ERF. B.3 is responsive to abiotic stresses and mediates salt and cold stress response regulation in tomato. Sci. World J. 2014, 167681.

Plant Life under Changing Environment

572

21. Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects

Koo, A.J., Howe, G.A., 2007. Role of peroxisomal beta-oxidation in the production of plant signalling compounds. Plant Signal Behav. 2, 20
22. Kramell, R., Miersch, O., Atzorn, R., Parthier, B., Wasternack, C., 2000. Octadecanoid-derived alteration of gene expression and the “oxylipin signature” in stressed barley leaves. Implications for different signalling pathways. Plant Physiol. 123, 177
187. Kubigsteltig, I., Laudert, D., Weiler, E.W., 1999. Structure and regulation of the Arabidopsis thaliana allene oxide synthase gene. Planta 208, 463
471. Kumar, J., Singh, V.P., Prasad, S.M., 2015. NaCl-induced physiological ad biochemical changes in two cyanobacteria Nostoc muscorum and Phormidium foveolarum acclimatized to different photosynthetically active radiation. J. Photochem. Photobiol. B: Biol. 151, 221
232. Kurepin, L.V., Joo, S.H., Kim, S.K., Pharis, R.P., Back, T.G., 2012. Interaction of brassinosteroids with light quality and plant hormones in regulating shoot growth of young sunflower and Arabidopsis seedlings. Plant Growth Regul. 31, 156
164. Kwak, J.M., Mori, I.,C., Pei, Z.M., Leonhardt, N., Torres, M.A., Dangl, J.L., et al., 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623
2633. Available from: https://doi.org/10.1093/emboj/cdg277. PMID: 12773379. Kyriakis, J.M., App, H., Zhang, X.F., Banerjee, P., Brautigan, D.L., Rapp, U.R., et al., 1992. Raf-1 activates MAP kinase-kinase. Nature 358, 417
421. Lechner, E., Achard, P., Vansiri, A., Potuschak, T., Genschik, P., 2006. F-boxproteins everywhere. Curr. Opin. Plant Biol. 9, 631
638. Lee, S., Suh, S., Kim, S., Crain, R.C., Kwak, J.M., Nam, H.-G., et al., 1997. Systemic elevation of phosphatidic acid and lyso-phospholipid levels in wounded plants. Plant J. 12, 547
556. Lee, S.C., Luan, S., 2012. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant, Cell Environ. 35, 53
60. Leon, J., Rojo, E., Sanchez-Serrano, J.J., 2001. Wound signaling in plants. Exp. Bot. 52, 1
9. Li, J.M., Chory, J., 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929
938. Li, L., Li, C.Y., Howe, G.A., 2001. Genetic analysis of wound signaling in tomato. Evidence for a dual role of jasmonic acid in defense and female fertility. Plant Physiol. 127, 1414
1417. Liu, Q., Yang, J.L., He, L.S., Zheng, J., 2008. Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale. Biol. Plant. 52, 87
92. Lovegrove, A., Barratt, D.H.P., Beale, M.H., Hooley, R., 1998. Gibberellin-photoaffinity labelling of two polypeptides in plant plasma membranes. Plant J. 15, 311
320. Luschnig, C., Gaxiola, R.A., Grisafi, P., Fink, G.R., 1998. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175
2187. Madhan, M., Mahesh, K., Rao, S.R., 2014. Effect of 24-epibrassinolide on aluminium stress induced inhibition of seed germination and seedling growth of Cajanus cajan (L.) Millsp. Int. J. Multidiscip. Curr. Res. 2, 286
290. Magome, H., Yamaguchi, S., Hanada, A., Kamiya, Y., Oda, K., 2008. The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivated gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J. 56. Available from: https://doi.org/10.1111/j.1365-313X.2008.03627.x. Mahajan, S., Tuteja, N., 2005. Cold, salinity and drought stress: an overview. Arch. Biochem. Biophys. 444, 139
158. Mahesh, B., Parshavaneni, B., Ramakrishna, B., Rao, S.S.R., 2013. Effect of brassinosteroids on germination and seedling growth of radish (Raphanus sativus L.) under PEG-6000 induced water stress. Am. Plant Sci. 4, 2305
2313. Mano, Y., Nemoto, K., 2012. The pathway of auxin biosynthesis in plants. Exp. Bot. 63, 2853
2872. Marcinkowska, E., Wiedlocha, A., 2002. Steroid signal transduction activated at the cell membrane: from plants to animals. Acta Biochem. Pol. 49, 735
745. Masood, A., Iqbal, N., Khan, N.A., 2012. Role of ethylene in alleviation of cadmium
induced photosynthetic capacity inhibition by sulphur in mustard. Plant Cell Environ. 35, 524
533. McAinsh, M.R., Brownlee, C., Hetherington, A.M., 1997. Calcium ions as second messengers in guard cell signal transduction. Physiol. Plant. 100, 16
29. McDonald, A., Riha, S., DiTommasob, A., DeGaetanoa, A., 2009. Climate change and the geography of weed damage: analysis of U.S. maize systems suggests the potential for significant range transformations. Agric. Ecosyst. Environ. 130, 131
140.

Plant Life under Changing Environment

References

573

McGinnis, K.M., Thomas, S.G., Soule, J.D., Strader, L.C., Zale, J.M., Sun, T.P., et al., 2003. The Arabidopsis SLEEPY1 gene encodes putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15, 1120
1130. Metraux, J.P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., et al., 1990. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004
1006. Metwally, A., Finkemeier, I., Georgi, M., Dietz, K.-J., 2003. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant. Physiol. 132, 272
281. Miersch, O., Wasternack, C., 2000. Octadecanoid and jasmonate signalling in tomato (Lycopersicon esculentum Mill.) leaves: endogenous jasmonates do not induce jasmonate biosynthesis. Biol. Chem. 381, 715
722. Milone, M.T., Sgherri, C., Clijsters, Navari-lazzo, F., 2003. Antioxidative responses of wheat treated with realistic concentration of cadmium. Environ. Exp. Bot. 50, 265
276. Mittler, R., 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15
19. Montoya, T., Nomura, T., Farrar, K., Kaneta, T., Yokota, T., Bishop, G.J., 2002. Cloning the tomato curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell 14, 3163
3176. Mueller, M.J., Brodschelm, W., Spannagl, E., Zenk, M.H., 1993. Signalling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc. Natl. Acad. Sci. U.S.A. 90, 7490
7494. Nishiyama, R., Watanabe, Y., Fujita, Y., Tien, L.D., Kojima, M., Werner, T., et al., 2011. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23, 2169
2183. Noctor, G., Veljovic-Jovanovic, S., Driscoll, S., Novitskaya, L., Foyer, C.H., 2002. Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann. Bot. 89, 841
850. O’Brien, J.A., Benkova, E., 2013. Cytokinin cross-talking during biotic and abiotic stress responses. Front. Plant Sci. 4, 451. Ouellet, F., Overvoorde, P.J., Theologis, A., 2001. IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13, 829
842. Ouzounidou, G., Ilias, I., 2005. Hormone-induced protection of sunflower photosynthetic apparatus against copper toxicity. Biol. Plant. 49 (2), 223
228. ¨ zdemir, F., Bor, M., Demiral, T., Turkan, I., 2004. Effects of 24-epibrassinolide on seed germination, seedling O growth, lipid peroxidation, proline content and antioxidative system of rice (Oryza sativa L.) under salinity stress. Plant Growth Regul. 42, 203
211. Panda, S.K., Singh, L.B., Khan, M.Z., 2003. Does aluminium phytotoxicity induce oxidative stress in greengram (Vigna Radiata)? Bulg. J. Plant Physiol. 29, 77
86. Parchmann, S., Gundlach, H., Mueller, M.J., 1997. Induction of 12-oxo-phytodienoic acid in wounded plants and elicited plant cell cultures. Plant Physiol. 115, 1057
1064. Parida, A.K., Das, A.B., 2005. Salt tolerance and salinity effect on plants: a review. Ecotoxicol. Environ. Saf. 60, 324
349. Pathak, M.R., da Silva Teixeira, J.A., Wani, S.H., 2014. Polyamines in response to abiotic stress tolerance through transgenic approaches. GM Crops Food 5, 87
96. Peters, K., Breitsameter, L., Gerowitt, B., 2014. Impact of climate change on weeds in agriculture: a review. Agric. Sustain. Dev. 34, 707
721. Popova, L.P., Maslenkova, L.T., Yordanova, R.Y., Ivanova, A.P., Krantev, A.P., Szalai, G., et al., 2009. Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol. Biochem. 47, 224
231. Pospı´sˇ ilova´, J., 2003. Interaction of cytokinins and abscisic acid during regulation of stomatal opening in bean leaves. Photosynthetica 41, 49
56. Rahman, H., Sabreen, S., Alam, S., Kawai, S., 2005. Effects of nickel on growth and composition of metal micronutrients in barley plants grown in nutrient solution. J. Plant Nutr. 28, 93
404. Ramakrishna, B., Rao, S.S.R., 2012. 24-Epibrassinolide alleviated zinc-induced oxidative stress in radish (Raphanus sativus L.) seedlings by enhancing antioxidative system. Plant Growth Regul. 68, 249
259. Rao, M.V., Paliyath, G., Ormrod, D.P., 1995. Differential response of photosynthetic pigments, RUBISCO activity and RUBISCO protein of Arabidopsis thaliana exposed to UV-B and ozone. Photochem. Photobiol. 62, 727
735. Rhoads, D.M., McIntosh, L., 1991. Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott). Proc. Natl. Acad. Sci. U.S.A. 88, 2122
2126.

Plant Life under Changing Environment

574

21. Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects

Rhoads, D.M., McIntosh, L., 1992. Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell 4, 1131
1139. Rivas-San Vicente, M., Plasencia, J., 2011. Salicylic acid beyond defense: its role in plant growth and development. J. Exp. Bot. 62, 3321
3338. Sanghera, G.S., Wani, S.H., Hussain, H., Singh, N.B., 2011. Engineering cold stress tolerance in crop plants. Curr. Genomics 14, 30
43. Santino, A., Taurino, M., De Domenico, S., Bonsegna, S., Poltronieri, P., Pastor, V., et al., 2013. Jasmonate signaling in plant development and defense response to multiple (a) biotic stresses. Plant Cell Rep. 32, 1085
1098. Sato, T., Theologis, A., 1989. Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate synthase, the key enzyme for ethylene biosynthesis in plants. Proc. Natl. Acad. Sci. U.S.A. 86, 6621
6625. Scherm, H., Coakley, S.M., 2003. Plant pathogens in a changing world. Aust. Plant Pathol. 32, 157
165. Schilmiller, A.L., Koo, A.J., Howe, G.A., 2007. Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiol. 143, 812
844. Seo, H.S., Song, J.T., Cheong, J.J., Lee, Y.H., Lee, Y.H., Hwang, I., et al., 2001. Jasmonic acid carboxylmethyltransferase: a key enzyme for jasmonate regulated plant responses. Proc. Natl. Acad. Sci. U.S.A. 98, 4788
4793. Shahzad, B., Tanveer, M., Che, Z., Rehman, A., Cheema, S.A., Sharma, A., et al., 2018. Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review. Ecotoxicol. Environ. Saf. 147, 935
944. Sharma, P., Bhardwaj, R., 2007. Effect of 24-epibrassinolide on seed germination, seedling growth and heavy metal uptake in Brassica juncea L. Gen. Appl. Plant. Physiol. 33, 59
73. Sharma, Y.K., Leon, J., Raskin, I., Davis, K.R., 1996. Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense related transcripts and induced resistance. Proc. Natl. Acad. Sci. U.S.A 93, 5099
5104. Sharma, N., Abrams, S.R., Waterer, D.R., 2005. Uptake, movement, activity, and persistence of an abscisic acid analog (80 acetylene ABA methyl ester) in marigold and tomato. Plant Growth Regul. 24, 28
35. Sharma, I., Pati, P.K., Bhardwaj, R., 2011. Effect of 28-homobrassinolide on antioxidant defence system in Raphanus sativus L. under chromium toxicity. Ecotoxicology 20, 862
874. Shaterian, J., Waterer, D., De Jong, H., Tanino, K.K., 2005. Differential stress responses to NaCl salt application in early- and late maturing diploid potato (Solanum sp.) clones. Environ. Exp. Bot. 54, 202
212. Shen, G., Niu, J., Deng, Z., 2017. Abscisic acid treatment alleviates cadmium toxicity in purple flowering stalk (Brassica campestris L. ssp. Chinensis var. purpurea Hort.) seedlings. Plant Physiol. Biochem. 118, 471
478. Silverstone, A.L., Chang, C.W., Krol, E., Sun, T.P., 1997. Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant 12, 9
19. Singh, G., Kaur, M., 1980. Effect of growth regulators on padding and yield of mung bean (Vigna radiata L.) Wilczek. Indian J. Plant Physiol. 23, 366
370. Singh, A., Prasad, S.M., 2014. Effect of agro-industrial waste amendment on Cd uptake in Amaranthus caudatus grown under contaminated soil: an oxidative biomarker response. Ecotoxicol. Environ. Saf. 100, 105
113. Singh, S., Prasad, S.M., 2015. IAA alleviates Cd toxicity on growth, photosynthesis and oxidative damages in eggplant seedlings. Plant Growth Regul. 77 (1), 87
98. Singh, S., Singh, A., Bashri, G., Prasad, S.M., 2015. Impact of Cd stress on cellular functioning and its amelioration by phytohormones: an overview on regulatory network. Plant Growth Regul. Available from: https://doi. org/10.1007/s10725-016-0170-2. Singh, S., Tripathi, D.K., Singh, S., Sharma, S., Dubey, N.K., Chauhan, D.K., 2017. Toxicity of aluminium on various levels of plant cells and organism: a review. Environ. Exp. Bot. 137, 177
193. Spanu, P., Reinhardt, D., Boller, T., 1991. Analysis and cloning of the ethylene-forming enzyme from tomato by functional expression of its mRNA in Xenopus laevis oocytes. EMBO J. 10, 2007
2013. Sreenivasulu, N., Harshavardhan, V.T., Govind, G., Seiler, C., Kohli, A., 2012. Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506, 265
273. Sripinyowanich, S., Klomsakul, P., Boonburapong, B., Bangyeekhun, T., Asami, T., Gu, H., et al., 2013. Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): the role of OsP5CS1 and OsP5CR gene expression during salt stress. Environ. Exp. Bot. 86, 94
105.

Plant Life under Changing Environment

References

575

Szekeres, M., 2003. Brassinosteroid and systemin: two hormones perceived by the same receptor. Trends Plant Sci. 8, 102
104. Tiwari, S.B., Hagen, G., Guilfoyle, T., 2003. The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15, 533
543. Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., Itoh, H., Katoh, E., Kobayashi, M., et al., 2005. Gibberellin insensitive dwarf1 encodes a soluble receptor for gibberellin. Nature 437, 693
698. Valerio, M., Lovelli, S., Perniola, M., Di Tommaso, T., Ziska, L., 2013. The role of water availability on weed
crop interactions in processing tomato for southern Italy. Acta Agric. Scand. Sect. B 63, 62
68. Vardhini, B.V., Anjum, N.A., 2015. Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system. Front. Environ. Sci. 2, 1
16. Vassilev, A., Yordanov, L., 1997. Reductive analysis of factors limiting growth of cadmium- treated plants: a review. Bulg. J. Plant Physiol. 23, 114
133. Vazquez, M.N., Guerrero, Y.R., Gonzalez, L.M., Noval, W.T., 2013. Brassinosteroids and plant responses to heavy metal stress: an overview. Open J. Metal. 3, 34
41. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, E., Ward, S., et al., 1994. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6 (7), 959
965. Vijayan, P., Shockey, J., Levesque, C.A., Cook, R.J., Browse, J., 1998. A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 95, 7209
7214. Vitorello, V.A., Capaldi, F.R., Stefanuto, V.A., 2005. Recent advances in aluminum toxicity and resistance in higher plants. Braz. J. Plant Phys. 17, 129
143. Wang, L., Wu, J., 2013. The essential role of jasmonic acid in plant-herbivore interactions
using the wild tobacco Nicotiana attenuata as a model. J. Genet Genomics 40, 597
606. Wang, Y., Mopper, S., Hasentein, K.H., 2001. Effects of salinity on endogenous ABA, IAA, JA, and SA in Iris hexagona. Chem. Ecol. 27, 327
342. Wang, X.H., Shu, C., Li, H.Y., Hu, X.Q., Wang, Y.X., 2014. Effects of 0.01% brassinolide solution application on yield of rice and its resistance to autumn low-temperature damage. Acta Agric. Jiangxi. 26, 36
38. Wani, S.H., Kumar, V., Shriram, V., Sah, S.K., 2016. Phytohormones and there metabolic engineering for abiotic tolerance in crop plants. Crop J. 4, 162
176. Wasternack, C., 2014. Action of jasmonates in plant stress responses and development—applied aspects. Biotechnol. Adv. 32 (1), 31
39. Wildermuth, M.C., Dewdney, J., Wu, G., Ausubel, F.M., 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562
565. Wilkinson, S., Kudoyarova, G.R., Veselov, D.S., Arkhipova, T.N., Davies, W.J., 2012. Plant hormone interactions: innovative targets for crop breeding and management. J. Exp. Bot. 63, 3499
3509. World Health Organization, 2007. Joint FAO/WHO Expert Standards Program Codex Alimentation Commission. Geneva, Switzerland. ,http://www.who.int. (accessed 10.09.12.). Worley, C.K., Zenser, N., Ramos, J., Rouse, D., Leyser, O., Theologis, A., et al., 2000. Degradation of Aux/IAA proteins is essential for normal auxin signalling. Plant 21, 553
562. Wu, Y., Sanchez, J.P., Lopez-Molina, L., Himmelbach, A., Grill, E., Chua, N.H., 2003. The abi1-1 mutation blocks ABA signaling downstream of cADPR action. Plant J. 34, 307
315. Wu, Y., Zhang, D., Chu, J.Y., Boyle, P., Wang, Y., Brindle, I.D., 2012. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 1, 639
647. Xiang, C., Oliver, D.J., 1998. Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10, 1539
1550. Xu, Y., Zhang, Y., Li, Y., Li, G., Liu, D., Zhao, M., et al., 2012. Growth promotion of Yunnan pine early seedlings in response to foliar application of IAA and IBA. Int. J. Mol. Sci. 13, 6507
6520. Xu, F., Xi, Z.M., Zhang, C.J., Zhang, Z.W., 2015. Brassinosteroids are involved in controlling sugar unloading in Vitis vinifera ‘Cabernet Sauvignon’ berries during ve´raison. Plant Physiol. Biochem. 94, 197
208. Yalpani, N., Silverman, P., Wilson, T.M.A., Kleier, S.A., Raskin, I., 1991. Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3, 809
818. Yamaguchi, S., 2008. Gibberellin metabolism and its regulation. Annu. Rev. Plant Physiol. 59, 225
251.

Plant Life under Changing Environment

576

21. Phytohormonal metabolic engineering for abiotic stress in plants: New avenues and future prospects

Yan, Y., Stolz, S., Che´telat, A., Reymond, P., Pagni, M., 2007. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19, 2470
2483. Yan, Z., Chen, J., Li, X., 2013. Methyl jasmonate as modulator of Cd toxicity in Capsicum frutescens var. fasciculatum seedlings. Ecotoxicol. Environ. Saf. 98, 203
209. Yang, S.F., Hoffman, N.E., 1984. Ethylene biosynthesis and its regulation in higher-plants. Annu. Rev. Plant Physiol. Plant Mol. Biol 35, 155
189. Yoon, J.Y., Hamayun, M., Lee, S.K., Lee, I.J., 2009. Methyl jasmonate alleviated salinity stress in soybean. J. Crop. Sci. Biotechnol. 12, 63
68. Yuan, S., Lin, H.H., 2008. Role of salicylic acid in plant abiotic stress. Z. Naturforsch. C 63, 313
320. Zhang, M.C., Zhai, Z.X., Tian, X.L., Duan, L.S., Li, Z.H., 2008. Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean (Glycine max L.). Plant Growth Regul. 56, 257
264. Zhang, Z.J., Li, F., Li, D.J., Zhang, H.W., Huang, R.F., 2010. Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232, 765
774. Zhang, Y., Xu, S., Yang, S., Chen, Y., 2015. Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252 (3), 911
924. Zholkevich, V.N., Pustovoytova, T.N., 1993. The role of Cucumis sativum L. leaves and content of phytohormones under soil droughts. Russ. Plant Physiol. 40, 676
680. Ziska, L.H., Tomecek, M.B., Gealy, D.R., 2010. Evaluation of competitive ability between cultivated and red weedy rice as a function of recent and projected increases in atmospheric CO2. Agron 102, 118
123. Zobel, R.W., Kinraide, T.B., Baligar, V.C., 2007. Fine root diameters can change in response to changes in nutrient concentrations. Plant Soil 297, 243
254.

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22 Abiotic-stress tolerance in plants-system biology approach Poonam Pandey, Sarita Srivastava, Akhilesh Kumar Pandey and Rama Shanker Dubey Department of Biochemistry, Institute of Science, Banaras Hindu University, Varanasi, India

22.1 Introduction Abiotic stresses of the environment, such as soil salinity, drought, extreme temperatures (heat and cold), light, water supply, nutrient deficiency, excess levels of metals within the soil, negatively impact plant growth. Agriculture faces intolerable economic losses wherever stress-related alterations in plant development, growth and productivity ultimately results in limited yield. Soil salinity and water scarcity (drought), problems exist in India, Argentina, China, the United States, Sudan, and many other countries in Western and Central Asia. Field crop estimation showed that it is almost all crops give best result only reaching 30% of the genetic potential for yield but over 90% of global rural land area is considered affected globally by abiotic stresses during the growing season. Most common responses to abiotic stresses in plants include differential transcription of the many genes, production of stress-responsive genes leading to cellular metabolic changes, alteration in activity behavior of many enzymes, overproduction of several compatible metabolites such as amino acids, sugars, polyamines, phytochelatins, organic acids; increased synthesis of many enzymes and stress-specific proteins. These specific responses to stresses have served as basis to engineer crop plants suitable for cultivation in the stress-prone regions of the world. Generally, plants are affected by low and moderate levels of abiotic stresses, but when the intensity of stress increases, tolerance mechanism of plants start breaking down that might ultimately result into death of the plant. To satisfy the increasing demand of food of the developing and underdeveloped nations where abiotic stresses are severe constraints to crop productivity, development of stress tolerant plants appear to be a propitious approach. Several biochemical, physiological, and metabolic strategies are developed in plants to combat such abiotic stresses. Often it is hard to foresee the complex

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signaling pathway that are activated or deactivated in response to various abiotic stresses (Chawla et al., 2011). New biotechnological methods should be adopted by plant breeders to accelerate breeding program. Specifically, breeders must emphasize on increasing the tolerance of crops to abiotic stresses (Tester and Langridge, 2010). Development of crop species with increasing yield below stress environment can be possible by the use of modern genetic engineering tools which help in selection across multiple traits and reduce cost and time. It is a big challenge to current agriculture biotechnology to fulfill increasing demand in food production due to constant increase in world population which may achieve 9 billion by 2050. Responses of crop plants in a systems biology manner will be helpful to build networks or models that will give better understanding of varied responses of crop plants to a dynamic environment which empowering us to outline the best engineering strategy for the development of enhanced abiotic stress tolerant crop species. Systems biology is an imminent field in the area of plant science going for coordinating information from various high throughput “omics” platforms, for example, transcriptome, metabolome, proteome, and genomics to comprehend the regulatory structure and association of plant responses and their inherent components (Moreno-Risueno et al., 2010; Cramer et al., 2011). They give new bits of knowledge and open new horizons for the better understanding of stresses and responses and also the improvement of plant responses and its resistance to stresses (Duque et al., 2013). Because of the vast-scale nature of these approaches, bioinformatics and computational approaches are highly connected with the above for either developing new data analytical methods, better visualization, or storage in sustainable online resources (Helmy et al., 2011, 2012a). Omic technologies have been used in substantial researches as a way to identify imperative intermediates controlling stress tolerance and as a tool to screen for variation in plants (Mochida and Shinozaki, 2010). The outcomes obtained by utilizing these approaches would then be able to be delivered using genetic transformation. The present chapter focuses on current status of knowledge related to abiotic stresses, their impact on plant growth and metabolism and the fundamentals of systems biology, the data and tools required for systems biology research and also highlighting the significance of the system biology approach for identifying molecular regulatory networks leading to a better adaptation capacity of crops to abiotic stresses.

22.2 Abiotic stresses and their impact on plant growth and metabolism Abiotic stresses cause detrimental effects on survival, biomass production, accumulation, and grain yield of most crops. They are the prime cause of losses in substantial agricultural production worldwide (Athar and Ashraf, 2009). Drought, salinity, high levels of metals in soil, and extreme temperatures are the major environmental factors among all abiotic-stress factors that modern agriculture has to subsist. Approximately, 50% 70% yield reduction in major crop plants are caused by them. Though severity of yield losses depends upon the intensity and duration of stress as well as plant species and its phase of growth (Jaleel et al., 2008). Some of the most common responses that are triggered in plants subjected to different abiotic stresses include alteration in gene expression, anatomical and morphological modifications, decreased efficiency of photosynthesis, decreased

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N assimilation capability, altered activities of many key enzymes and plasma membrane characteristics, cellular metabolic adjustments, overproduction of many metabolites, and increased synthesis of stress-induced novel proteins (Fig. 22.1). Among these abiotic stresses, drought (water stress) is the most acute, responsible for declined agricultural production worldwide. It influences plants in a few different ways: plant growth and development, loss of membrane integrity, stomatal closure, pigment content, osmotic alterations, water relations, limit photosynthetic activity by diminishing CO2 influx, accumulation of Abscisic acid (ABA), osmolytes proline, mannitol, sorbitol, formation of radical scavenging compounds (ascorbate, glutathione, a-tocopherol, etc.), synthesis of new proteins and mRNAs (Osakabe et al., 2014) as well as decrease in carboxylation, and electron transport chain activities of the chloroplasts inside the mesophyll cells (Feller and Vaseva, 2014). Salinity is the second most damaging stress after drought which reduces crop productivity. High salt concentration causes adverse effects on processes, such as seed germination, seedling growth and vigor, vegetative growth, flowering and fruit set, eventually causing reduced economic yield and furthermore quality of produce. Osmotic stress and ionic toxicity are the two major effects induced by salinity (Munns and Tester, 2008). In salt stress due to the presence of more salt in salt solution, osmotic pressure of soil solution overshoots the osmotic pressure in plant cells and, thus, limits the ability of plants to

FIGURE 22.1 Abiotic stress induced common responses in plants. Plants have variable thresholds for stress tolerance. Plants try to tolerate stresses but severe stresses result in productivity loss and eventually death.

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take up water and minerals such as K1, Ca21, and Mn21. In the meantime, Na1 and Cl2 ions can go into the cells and have direct toxic effects on cell membranes and additionally on metabolic activities in the cytosol. Osmotically stressed plants show some secondary effects such as assimilate production, reduced cell expansion, and membrane function, and also diminished cytosolic metabolism and ROS production. Salt stress causes altered enzyme activities. A significant enhancement of superoxide dismutase, peroxidase, catalase, and phenylalanine ammonia-lyase, tryptophan decarboxylase activity was reported in salt-stressed plants (Gao et al., 2008; Mishra et al., 2013). Due to global warming, temperature of global surface is rising continuously, heat stress is becoming an important agricultural problem, which is truly affecting the growth and production of plants, particularly crops. Inhibition in percentage of seed germination, loss in photosynthetic efficiency and respiration, and decrease in membrane permeability are observed during heat stress in plants (Mathur and Jajoo, 2014). Increased temperature prevent the swelling of pollen grains during flowering and results in poor release of pollen grains and the anther indehiscence, as well as during the reproductive growth period, the functions of the tapetal cells are lost, and the anther is dysplastic. Heat stress caused major responses such as alterations in the level of phytohormones, primary and secondary metabolites, enhancement in the expression of heat shock and related proteins, and production of reactive oxygen species (ROS) in plants (Camejo et al., 2006). Presence of excess amounts of different essential metals and metal pollutants in agricultural soils has also been the matter of greater concern during the last few decades. Metals when present in overabundance in the soil create considerable stress in growing plants and adversely affect crop productivity. Metal toxicity in plants includes their direct interaction with proteins, enzymes, causes displacement of essential cations from specific binding sites, leading to altered metabolism in the tissues due to alteration in the activities of key enzymes of metabolic pathways (Sharma and Dubey, 2007; Sharma and Dietz, 2009; Dubey, 2011). The response of plants toward metals is variable and relies upon the development phase of plants together with the concentration of metals and duration of exposure (Srivastava and Dubey, 2011). Exposure to heavy metals such as cadmium and mercury caused a decrease in germination percentage, germination index, and seedling length (Peng et al., 2010). Three different molecular mechanisms of heavy metal toxicity can be distinguished based on their chemical and physical properties: (1) blocking of basic functional groups in biomolecules, (2) displacement of essential metal ions from biomolecules, (3) production of ROS (Schu¨tzendu¨bel and Polle, 2002). A wide array of metabolic alterations has been reported in metal-stressed plants. Arsenic alters the activities of proteolytic, nucleolytic, and phosphorolytic enzymes in growing rice plants (Mishra and Dubey, 2008) and hinders the activities of several enzymes, for example, acid phosphatase, ribonuclease, glucose 6 phosphate dehydrogenase, malic enzyme, isocitrate dehydrogenase, RuBisCO, and carbonic anhydrase. Ni toxicity suppresses the hydrolysis of RNA and proteins by restraining the activity of RNase and protease, respectively, in rice seedlings (Maheshwari and Dubey, 2007). To establish an agricultural improvement and to satisfy the increased food requirement of global population, it is necessary to mitigate the effects of abiotic stress (Tester and Langridge, 2010), but enhancing plant wellness over a more extensive scope of environmental conditions would take into consideration an expanded use of degraded or marginal lands for agricultural production. To attain these objectives, one requires an essential

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and basic comprehension of the physiological and metabolic techniques utilized by plants to acquire the phenotypic plasticity required to limit damage and withstand the numerous and often overlapping adverse growth conditions that they can face once a day.

22.3 Systems biology approaches for improvement of plant’s abiotic-stress tolerance The integration of genes, metabolites, proteins, regulatory elements, and other biological components associated with stress adaptation and tolerance is studied under systems biology by using models as well as networks based on interactions among biological components. Agricultural scientists have been using system approaches to explore whole-crop physiology, crop ecology, and morphology (Trewavas, 2006). It requires the development of tools in order to (1) collect qualitative and quantitative information on many elements of the system, at the entire genome scale when attainable, and for various sorts of cell components, for example, the genes, RNAs, proteins or metabolites, (2) the recreation of models which are formal explanations of the components of the system and the communications between them. These models ought to be convertible in mathematical format, and (3) computational algorithms ought to have the capacity to calculate in a sensible computational time the behavior of such complex systems, based on the experimental data collected and the model canvas (Sauer et al., 2007; Peyraud et al., 2017). Systems biology has emerged as an extensively utilized methodology with the advancement of the purported “omics” techniques and the spectacular progress in techniques for the characterization of the principal components of the cell in the last two decades: DNA and RNA sequencing for genes, and mass spectrometry (MS) for proteins and metabolites (Metzker, 2010; Altelaar et al., 2013). They give new insights and open new perspectives for understanding stresses and responses and in addition the enhancement of plant responses and protection from stresses (Duque et al., 2013) (Fig. 22.2). In the following sections the “parts” of plant systems biology (omics approaches), its principal technologies, and predicted results have been described.

22.3.1 Genomics Genomics is the study of all the genes in a given genome together with the identification of gene sequences, intragenic sequences, gene structures, and annotations (Duque et al., 2013). An enormous development within the discipline of genomics in the ultimate 20 years has driven a more profound comprehension in the area, as an example, gene expression, organization, and its relationship to stress resistance. Comparative genomics and techniques, for example, high-throughput analysis of expressed sequence tags, largescale parallel analysis of gene expression, targeted or random mutagenesis, and advantage-of-feature or mutant complementation, disclosure of novel genes, determination of their expression patterns in response to abiotic stress, and a better knowledge of their roles in stress adaptation (acquired by using the utilization of functional genomics) will give the premise of powerful engineering techniques resulting in greater stress tolerance

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FIGURE 22.2 Schematic overview of the systems biology approaches and their advancements as well as expected results in studying abiotic stress responses in plants.

(Cushman and Bohnert, 2000). Molecular understanding of the stress observation, signal transduction, and transcriptional regulation of various abiotic stress responsive genes may facilitate in engineering the tolerance of crop plants to multiple stresses. Some specific requirements for genome analysis of model plants are (1) small genome size, (2) short generation time, (3) small size to empower development to restricted space, and (4) accessibility of gene manipulation technologies (Tabata, 2002). There are a few model systems available in plants. Among all of them, thale cress (Arabidopsis thaliana) and rice (Oryza sativa L.) are the two most important model species for dicotyledonous and monocotyledonous plant species, respectively. Currently, two basic genetic approaches being employed to enhance stress tolerance consist of (1) utilization of natural genetic variations, either through direct selection in stressful environments or through the mapping of quantitative trait loci (QTL) and consequent marker-assisted selection and (2) generation of

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transgenic plants to introduce novel genes or alter expression levels of the present genes to influence the level of abiotic-stress tolerance (Blumwald et al., 2004). An essential advantage of QTL-based processes is that they might also permit manufacturing of stresstolerant crops through combining or “pyramiding” QTLs for various stress tolerances. Several researches had been carried out to identify QTL conferring resistance to abiotic stresses and to narrate QTLs to physiological tolerance mechanisms (Collins et al., 2008; Wu et al., 2014; Fan et al., 2015). A SNAC1 gene and late-embryogenesis-abundant (LEA) gene was once identified from microarray experiments that induced the expression of a range of stress-tolerance genes and enhanced the drought and salt resistance of rice in the field (Hu et al., 2006; Xiao et al., 2007). Overexpression of ZFP245 and OsWRKY30 has been observed to amplify tolerance to drought and low-temperature stresses in rice plants (Huang et al., 2009; Shen et al., 2012). In current years, genome-editing tools give a technique to introduce targeted adjustments in the genome successfully to observe the functional aspects of different components of the genome in various plants and offer potential avenues for manufacturing of abiotic stress-tolerant crops. Zinc finger nucleases, transcriptional activator-like effector nucleases, and clustered regularly interspaced short palindromic repeat (CRISPR)-Cas9 (CRISPR-associated nuclease 9) are the most generally used genome-editing tools (Voytas, 2013; Kumar and Jain, 2014). The advancement of novel regulatory module(s) from normally existing components (genes, promoters, cis-regulatory elements, small RNAs, and epigenetic alterations) can encourage the engineering of signaling/regulatory and metabolic procedures to balance plant’s abiotic-stress tolerance. Few investigations have exhibited the assembly of homozygous transgenic plants inside the first generation and its steady transmission to progressive generations (Feng et al., 2013; Brooks et al., 2014; Zhang et al., 2014a,b) that presented the quickest feasible approach throughout a crop plant genome modification. These procedures will decrease breeding or gene transformation time significantly for generation of new varieties/transgenic plants with preferred qualities.

22.3.2 Transcriptomics Transcriptome refers to the set of all the genomic counterparts which are expressed as RNA transcripts, such as protein coding (mRNA) and noncoding RNAs (tRNA, rRNA, miRNA, etc.) at a given time in a cell or population of cells under a particular set of environmental conditions (Wang et al., 2010). Transcriptomics generally helps in discovering abiotic stress candidate genes that add to stress tolerance via the evaluation of transcriptomes of the similar plant under optimal and stress conditions (Le et al., 2012; Zhang et al., 2014a,b). Conventional transcriptional analyses included northern blots; however, the introduction of high-throughput technologies has empowered us to explain the whole transcriptome of model and nonmodel plants. The advanced techniques for transcriptome explanation incorporate microarray analysis and next-generation sequencing (NGS) technologies. Genome-wide measurement of transcript levels by using microarrays gives a promising methodology toward the identification and functional evaluation of genes underlying multiple-stress tolerance (Clarke and Zhu, 2006). Zhu et al. (2013) carried out a comparative microarray analysis approach to learn about the transcriptome changes of

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cotton in five abiotic stresses. Their study revealed the functional genes and stress-related pathways and furthermore proposed a crosstalk of responsive genes or pathways to more than one abiotic stresses in cotton seedlings. An assortment of bioinformatics tools have exuded in the microarray-based research of the plant group, namely, Genevestigator (Zimmermann et al., 2004), NASCArrays (Craigon et al., 2004), ArrayExpress (Parkinson et al., 2005), the Gene Expression Omnibus (Edgar et al., 2002), and Stanford Microarray Database (Ball et al., 2005). The NGS technologies in RNA-seq are a prominent way to deal with accumulating and quantifying the vast-scale sequences of coding and noncoding RNA pools at a low cost (Wang et al., 2009a,b; Garber et al., 2011). Recently, many studies have shown that RNA-seq has given a valuable tool for identification of related genes and their expression patterns in crop pests and plant species reacting to a few biotic and abiotic stresses (Nachappa et al., 2012; Yu et al., 2012). Wakasa et al. (2014) recently generated transgenic rice plants, made by homologous recombination, within which single copy of genomic OsIRE1 (ER stress sensor/transducer) was supplanted by two kinds of missense alleles imperfect in RNase activity. This study gave profitable data about the ER stress response in rice plants and prompted the revelation of new genes related with ER stress. Various bioinformatics tools help the de novo assembly in RNA-seq-based applications, namely, CAP3 (Huang and Madan, 1999), CLC bio Genomics Workbench (CLC Bio), MIRA (Chevreux et al., 2004), Trinity (Grabherr et al., 2011), and Velvet (Zerbino and Birney, 2008). Increasing the availability of online resources, databases, and series of transcriptome information allow novel genome-wide study of plant’s stress tolerance and responses (Duque et al., 2013; Jogaiah et al., 2013).

22.3.3 Proteomics Proteomics is the large-scale study of protein characteristics and functions. The objective of proteomics research is to acquire a coordinated perspective of normal and abnormal cellular processes at the level of their constituent proteins [for instance, in phrases of protein abundance, characterization of posttranslational modifications (PTMs), protein protein interactions (PPIs), and their regulatory networks] (Hashiguchi et al., 2010). Proteins show distinctive features underlying plant’s stress tolerance: they function as enzymes, display protective roles, bind water, have interaction with other proteins and biomolecules, scavenge ROS either directly through chemical reactions with certain amino acid residues or indirectly by means of metal cofactors. Proteomics is more complicated than genomics since genome is more or less steady in an organism, while proteome differs from cell to cell and with time. Proteomics is linked with two sorts of studies: (1) proteome profiling (the discovery of particular targets and markers) and (2) functional proteomics (the definition of structure, interactions, and function). Proteomic approach has been mostly adopted to check out the protein profiles in plants in response to abiotic stress, which may prompt the development of new techniques for enhancing stress tolerance (Rodziewicz et al., 2014; Barkla et al., 2016). Two-dimensional polyacrylamide gel electrophoresis (2D PAGE) is mainly compatible to protein-profiling studies. It also provides itself well to targeted (functional) proteomic studies, wherein the expression/change of specific proteins is accompanied through systematic treatment regimens or change in growth conditions.

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Organ-specific proteomics, combined with subcellular organelle proteomic studies, offer more detailed information for understanding cell systems that manage stress response and signal transduction in different organelles, and that they might be utilized to upgrade crop’s stress tolerance (Komatsu and Hossain, 2013; Yin et al., 2015). A lot of studies demonstrate that some stress-responsive proteins uncover dynamical changes in their abundance corresponding to changes in plant’s tolerance level upon stress (Abbasi and Komatsu, 2004; Gao et al., 2009; Chen et al., 2016). Diverse research coping with correlation of proteome changes in related genotypes uncovering differentiating reactions to a specific stress factor ought to result in identity of certain proteins underlying the observed variations among tolerant and sensitive genotypes. For examples, in cold-acclimated winter wheat WCS120 (Vı´ta´mva´s et al., 2007), a few sHSPs have been identified in heat-treated wheat grain throughout the grain-filling period (Skylas et al., 2002), Trx h and GST in drought-treated wheat grain (Hajheidari et al., 2007) or RuBisCO activase and Calvin cycle enzymes in drought-treated Populus 3 euramericana (Bonhomme et al., 2009). Comparative proteomic studies exploring mechanisms of Al resistance in rice revealed that the relative abundance of vacuolar H1-ATPase increased in Al tolerant rice cultivars contrasted with Al-sensitive cultivars, while structural proteins decreased in each cultivar (Wang et al., 2013). These differentially expressed proteins probably take into consideration the ability of protein biomarkers underlying tolerance to a given stress factor. Bioinformatics has immensely helped in the complete evaluation of the proteomic information. Diverse 2D PAGE-related databases are available on the internet such as ECO-2DBASE (VanBogelen et al., 1999), SWISS-2DPAGE (Hoogland et al., 2000), and WORLD-2DPAGE (especially for plant proteins). A few different programs are also accessible for the image analysis of the 2D gels such as Melanie (Appel et al., 1997), PDQuest (BioRad), Progenesis (Rosengren et al., 2003), and Delta 2D (Decodon GmbH). The protein mass fingerprinting evaluation tools consist of Mascot, Sequest, Aldente, Popitam, Phenyx, FindMod, Profound, PepFrag, MS-Fit, OMSSA, TagIdent, etc. The protein databases accessible on the web include Genbank, Ensembl, PIR, SwissProt/UniProt knowledgebase, Tr-EMBL, and EST database (Vihinen, 2001).

22.3.4 Metabolomics Genomics, transcriptomics, and proteomics facilitate in distinguishing the candidate genes and proteins participating in critical roles in plant’s stress responses. However, the depiction of the regulatory networks and metabolic pathways reacting to single and numerous simultaneous stresses is required for better understanding stress response in crop plants. Within the previous few years, metabolomics gave another peak to stress associated studies and have turned into an essential tool in understanding the molecular mechanisms underlying stress responses (Weckwerth and Kahl, 2013). Metabolomics corresponds to a field of study with which we are capable to gain a much better understanding of the complexity of biological systems. It manages the identification and quantification of all low molecular weight metabolites (,1500 Da) present in such systems (Cevallos-Cevallos et al., 2009), despite the fact that the range could be sometimes more extensive (30 3000 Da) (Kim et al., 2011). The group of small molecules of metabolites that

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are in a cell, in an organ, or organism is referred to as metabolome (Wishart, 2008). It comprises a large variety of molecules, for example, peptides, amino acids, nucleic acids, carbohydrates, organic acids, vitamins, flavonoids, polyphenols, alkaloids, minerals, or some other chemical compound that is used, metabolized, or synthesized through a cell or by means of a given organism (Wishart, 2008). An expected 200,000 metabolites exist in plant (Pichersky and Gang, 2000), though just B50,000 have been explained (De Luca and St Pierre, 2000). Metabolic profiles give a biochemical phenotypic appraisal of the plants and hence are the most important in systems biology studies, so observed as a foundation of systems biology (Saito and Matsuda, 2010). Because of differences in the chemical and physical properties of the metabolites, a mixture of a few analytical and separation methods is required to attain the metabolic profile of a plant or given sample such as nuclear magnetic resonance (NMR), liquid chromatography NMR, MS: gas chromatography MS (GC MS), capillary electrophoresis MS, liquid chromatography MS, liquid chromatography electrochemistry MS, direct infusion MS, Fourier transform ion cyclotron MS (FTMS); infrared spectroscopy, thin layer chromatography, highperformance liquid chromatography equipped with various types of indicators: UV or photodiode array, fluorescent, electrochemical, etc., and Fourier transform infrared (Allwood and Goodacre, 2010; Jogaiah et al., 2013). Metabolomics is generally used in aggregate with other omics analysis (e.g., transcriptomics or proteomics) to explore the connection between metabolite levels and the expression level of genes/proteins (Srivastava et al., 2013). A solid correlation between stress metabolites and a specific gene/protein points out the function of this gene/protein in the response process (Urano et al., 2010; Jogaiah et al., 2013). Metabolomics is used to give a superior comprehension of the stress response and tolerance process in model plants, for example, Arabidopsis (Cook et al., 2004) and production crops such as the common bean (Phaseolus vulgaris) (Broughton et al., 2003), poplars (Populus 3 canescens) (Behnke et al., 2010), cereals (Sicher and Barnaby, 2012), and other food crops (Herna´ndez et al., 2007; Duque et al., 2013). An alternate report on rice roots used both GC MS and 1H-NMR metabolomics related to depth transcriptomic analysis in order to explain the impacts of chromium(VI) toxicity (Dubey et al., 2010). Different bioinformatics tools and databases are accessible for handling, preparing, and examining metabolomics information (Fukushima and Kusano, 2013).

22.3.5 Interactomics Interactomics involves the study of interaction of bioinformatics and biology that deals with analyzing both the interactions and also the effects of these interactions between and among proteins, and completely different molecules within a cell (Kiemer and Cesareni, 2007). PPIs are vital for nearly all biological functions mediated by using macromolecular machinery together with replisomes, spliceosomes, ribosomes, proteasomes, signalosomes, catalytic enzyme modules, signal recognition complexes, and specialized protein complexes distinctive to plants, for example, light harvesting and photosystem complexes. Thus distinguishing, quantifying, localizing, and modeling complete PPI networks (or “interactomes”) is essential for comprehension of the biophysical principle of every single cell process and for making a framework to represent the characteristics of all proteins (Sharan and Ideker, 2006).

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At the systems biology age, the buildup of PPI knowledge empowered the systems level study of protein interaction network. Indeed, there are numerous in vivo and in vitro technological platforms employed for the plant interactome mapping studies such as yeast two hybrid (Y2H), split-ubiquitin system, bimolecular fluorescence complementation, split-luciferase system, fluorescence resonance energy transfer (FRET), bioluminescence resonance energy transfer, and affinity purification MS (AP MS) (Morsy et al., 2008). The diverse PPI web resources in plants consist of rice kinase protein interaction map (Ding et al., 2009), Arabidopsis interactome 1 (Arabidopsis Interactome Mapping Consortium, 2011), Arabidopsis membrane interactome (Mukhtar et al., 2011), auxin signaling network (Vernoux et al., 2011), InAct (Aranda et al., 2009), The Arabidopsis Information Resource (TAIR) protein interaction data (Swarbreck et al., 2007), AtPID (Cui et al., 2007), CORNET (De Bodt et al., 2012), PAIR (Lin et al., 2011), PRIN (Gu et al., 2011), MINT (Licata et al., 2011), etc.

22.3.6 Other “omics” approaches In addition to the earlier-described principle omics approaches, some ongoing methodologies include lipidomics (complete analysis of lipids in biological systems) and hormonomics (the complete set of endogenous hormones throughout a plant) (Sheth and Thaker, 2014). The low molecular weight plant hormones comprise auxin, ABA, cytokinin, gibberellins, ethylene, brassinosteroids, jasmonates, salicylic acid, and a newly known one—strigolactone (acting as a shoot branching inhibitor) (Gomez-Roldan et al., 2008) and lectinomics (bioinformatics research of carbohydrate-binding proteins). Furthermore, another idea that has increased abundant attention during this time is that of phenomics, the high-throughput systemic measurement and analysis of qualitative and quantitative traits, and additionally scientific, biochemical, and imaging approaches, for the refinement and characterization of a phenotype (Houle et al., 2010).

22.4 Integration of multiple “omics” data Integration of the diverse omics data information studies has extraordinarily expanded our knowledge of plant reactions to different stresses. The effective combination of information will rely upon proper trial configuration, sound statistical analysis and, right translation of the outcomes. The different parts of fruitful incorporation of numerous heterogeneous omics datasets are to store individual “omics” information to particular public repositories, to produce connections among fluctuated sorts of datasets, representation of the information, and use of measurable and bioinformatics assets, where and when required (Bu¨low et al., 2006) (Fig. 22.3). A few research groups have given work processes to coordinate this information into one pipeline.

22.4.1 Transcriptomic proteomic A repeated issue in transcriptomics and proteomics is the connection between the expression of protein-coding genes and the plenitude of the corresponding proteins. Plant Life under Changing Environment

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FIGURE 22.3 General outline of a typical plant systems biology approach for integration of data, modelling and computational simulation. A biological hypothesis is addressed and tested applying one or different stresses, using at least one omics technologies. Source: Modified from Sheth, B.P., Thaker, V.S., 2014. Plant systems biology: insights, advances and challenges. Planta 240 (1), 33 54

The integrated use of transcriptomic and proteomic information has been accounted for in various ongoing investigations, such as entire plant nitrogen economics of maize (Amiour et al., 2012), development to dormancy transition in white spruce stems (Galindo Gonzalez et al., 2012), phytohormone crosstalk (Proietti et al., 2013), and flour quality in wheat (Altenbach et al., 2010).

22.4.2 Transcriptomic metabolomic Another possibility is to coordinate transcription with metabolites. This integration may additionally facilitate in disclosing genes and procedures underlying complicated traits (Joung et al., 2009). Keeping in mind the end goal to encourage the integration, some software program packages are produced such as MapMan (Urbanczyk-Wochniak et al., 2006) and MetGenMap (Joosen et al., 2011). These programs have been effectively connected to identification of genes and involved in various metabolic pathways, for example, germination, diurnal cycles (Kempa et al., 2008), and seed dormancy (Luo et al., 2009). Integrated study of metabolome and transcriptome was as of late applied in investigation of ricedeveloping caryopses under high-temperature conditions (Yamakawa and Hakata, 2010), molecular events underlying pollination-induced and pollination-independent fruit sets (Wang et al., 2009a,b), the impacts of DE-ETIOLATED1 downregulation in tomato fruits (Enfissi et al., 2010) and consistently changing metabolic frameworks in plants developing in field conditions, for example, the rice mutant and transgenic barley (Kogel et al., 2010; Izawa et al., 2011).

22.4.3 Metabolomic proteomic In nontargeted metabolomics, principal component analysis (PCA) and independent component analysis are strategies normally used to perform design acknowledgment. Plant Life under Changing Environment

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Furthermore, its capability to fortify this strategy by including extra parameters, such as outside perturbations (stress), protein concentration, and/or enzyme activities, along these lines, produce metabolite correlation networks. Recently, a coordinated metabolome and proteome approach was carried out in wheat and rice coleoptiles to compare the varieties accordingly with anoxia (Shingaki-Wells et al., 2011) and characterization of starch and raffinose metabolisms to low and high temperatures in A. thaliana (Mostafavi et al., 2008). Also, there are numerous difficulties in the integration of various omics information (De Keersmaecker et al., 2006; Steinfath et al., 2007). In the case of proteomics and metabolomics, huge specialized difficulties exist in defeating the similar large-scale scope of the varied transcriptomics platforms, because of the various compound natures of each protein and metabolites, and therefore the difficulty of preamplification as inside the instance of nucleic acids, making instrument affectability a major test. The solutions to the present issue comprise building “information (data) warehouses,” utilization of extensible markup language, hypertext navigation, unmediated MultiDB queries, production of federated database, and using controlled vocabularies. These are cases of existing information warehouses: Atlas, BioMart, BioWarehouse, Columba, SYSTOMONAS, BioDWH, VINEdb, Booly, and GNCPro (Turenne, 2011). VirtualPlant (Ahuja et al., 2010) and GeneMANIA (Des Marais and Juenger, 2010) empower the combination of different substantial scale information to begin demonstrating the advanced behavior of organisms.

22.5 Modeling and simulation in plant system dynamics The successful modeling of the plants is the final objective of plant systems biology. In arithmetic, a model (modus in Latin, which implies way/measure) generally speaks to the causal connections in a system. In systems biology, cells or higher units of biological association are comprehended as frameworks of interacting components. For a systems level clarification, one must understand the identity of the constituents, dynamic conduct, and collaborations among the constituents, of the biological system, under investigation (Kitano, 2002). This information will eventually be combined into a model that will not only be consistent with the present knowledge, but will also be able to predict the behavior of the system under the new and unknown perturbations. For many years, researchers have utilized the thoughts and methodologies of these systems as powerful crop development reproduction models (“crop models” in future) to explore crop development predominantly in response to abiotic environmental factors. In recent years, attempts have been made to employ models to measure crop genotype phenotype connections (Yin et al., 2000, 2004; Hammer et al., 2006). Yin et al. (2000) reported that examining genotype phenotype connections requires heartier yield models than do traditional agricultural applications. A network/graph, in systems biology, has two fundamental parts: the components of the system are represented as graph nodes (also called vertices) and furthermore the interactions are represented as edges, that is, lines between pairs of nodes. In biological networks, vertices represent the molecules present inside a cell (e.g., proteins, RNAs as well as metabolites), and the edges between nodes represent their natural connections (e.g., physical

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interaction, regulatory connections, metabolic reactions) (Blais and Dynlacht, 2005). Network development and examination is a standout amongst the most widely recognized ways to deal with biological systems. Systems/Models can be either static or dynamic depending on their behavior in the system with time, and their segments can incorporate genes, proteins, cis-elements, metabolites, and other molecules. At this time, we focus around four network composes, including gene-to-metabolite, PPI, transcriptional regulatory, and gene regulatory networks. The initial three kinds of systems are regularly static, while the gene regulatory network often emphasizes the dynamic changes of procedures (Yuan et al., 2008).

22.5.1 Gene-to-metabolite networks Gene-to-metabolite networks characterize the connections among genes and metabolites and are normally built using multivariate investigation or data processing of gene and metabolite profiling information under a given set of conditions. The analysis of gene-tometabolite networks is more complicated and difficult to study in plants, especially in assessment with mammals, due to bigger diversity and larger numbers of metabolites delivered by plants as an adjustment to their sessile way of life. Scientists used gene-to-metabolite networks to analyze the dynamic reactions all through sulfur and nitrogen starvation in Arabidopsis (Hirai, et al., 2004; Hoefgen and Nikiforova, 2008). The work incorporated microarray-based gene profiling with liquid chromatography MS and FTMS-based metabolite profiling using multivariate investigation techniques together with PCA and self-organizing maps to get gene-to-metabolite associations (Nikiforova et al., 2005). Different new research measurements such as interrelation amongst biological processes, gene functional annotation, disclosure of new genes in biosynthesis, regulation and transport of metabolites, have been added to plant science inferable from the illustration of gene-to-metabolite networks (Yuan et al., 2008). The gene-to-metabolite networks have been worked out in different studies such as in stress responses plant defense and hormone-induced responses (Carrari et al., 2006; Zulak et al., 2007), revelation of novel candidate genes for terpenoid indole alkaloid biosynthesis in Catharanthus roseus (Rischer et al., 2006), and in the response to nitrogen deficiency and through diurnal cycles (Bla¨sing et al., 2005; Masclaux-Daubresse et al., 2010).

22.5.2 Protein protein interaction networks Interaction between proteins is an important part of systems biology. PPIs are involved in a wide range of biological processes, including cell-to-cell interactions as well as metabolic and developmental control. Indeed, some methods such as Y2H screening; FRET, and affinity purification of complexes followed by MS (AP MS) analysis were used to explain the plant PPI networks in an assortment of model species (Yuan et al., 2008). The comprehension of the plant PPI system will give significant insights into the control of plant developmental, physiological, and pathological processes. Two types of interactions may be possible: genetic or physical. Genetic PPI is a network of genes characterized on the basis of genetic interactions to enlighten gene function inside physiological processes

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(Yuan et al., 2008) though this approach is hard to execute owing to the ploidy levels and long life cycles of plants. In contrast, physical interactions are simpler to be described on the plant systems. The physical interaction between the proteins can be significant to an assortment of biological processes including signal transduction, homeostasis control, stress responses, plant defense, and organ configuration (Ding et al., 2009; Zhang et al., 2010). A PPI network of 73 proteins and 97 interactions has been prepared to examine the role of up- and downregulated stress responsive genes in wheat plants (Tardif et al., 2007). These studies give network scaffolds that assist in constructing signaling networks for understanding systemic regulation of biological processes (Uhrig, 2006). A few protein interaction databases, including DIP (Salwinski et al., 2004), BIND (Gilbert, 2005), BioGRID (Stark et al., 2006), IntAct (Kerrien et al., 2006), MINT (Chatr-Aryamontri et al., 2006), and AtPID (Cui et al., 2007), have developed to arrange, store, and make PPI information accessible for investigation by the research community.

22.5.3 Transcriptional regulatory networks The transcription regulatory network clarifies the regulatory connections between regulatory genes and genes located downstream to them. They have two kinds of nodes— transcription factors (TFs) and regulatory genes and two sorts of directed edged, namely, transcriptional regulation and translation (Babu et al., 2004). An assortment of methods to deal with decoding transcriptional regulatory networks include genome-wide expression profiling (to construct gene regulatory networks), genome-wide profiling approach through RNA interference, transcription rate assessment by measuring of mRNA decay rates, the analysis of promoter cooccupancy through pairs of TFs, and cis-element prediction (Sheth and Thaker, 2014). A few computational tools and databases have been created to differentiate the interaction among TFs and cis-elements, an essential part in the development of transcriptional regulatory networks (Palaniswamy et al., 2006). The TFs collaborate with cis-elements within the promoter regions of a few stress-related genes and therefore upregulate the expression of numerous downstream genes resulting in conferring abiotic-stress tolerance (Agarwal and Jha, 2010). Transcriptome analysis in Arabidopsis and in a wide range of plants recommend that there are numerous pathways that autonomously react to environmental stresses (both ABA dependent and independent modes), signifying that stress tolerance or susceptibility is managed by way of the transcriptional level through extremely intricate gene regulatory networks (Umezawa et al., 2006). Transcriptomic analysis of other cereal crops, which include barley (Talame et al., 2007), maize (Luo et al., 2010), and sorghum (Buchanan et al., 2005), has demonstrated that a huge number of genes are up- or downregulated under abiotic stress conditions. In this manner, study of transcriptional regulatory systems is imperative to illuminate abiotic stress responses and tolerance. ABA plays a vital role in abiotic stress responses of higher plants throughout vegetative growth. One of the ABA-mediated responses is induced expression of a large number of genes, mediated by cis-regulatory elements referred to as abscisic acid responsive elements (ABREs). Another transcription factors involved in abiotic stress responses in plants include the NAC-type transcription factors (TFs). The NAC (NAM, ATAF1 2, and CUC2) family of plant-specific TFs represents one of the most

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important and largest families of TFs in the plants. NAC has been derived from the names of first three described TFs containing NAC domain, namely NAM, ATAF1 2, and CUC2 with 150 amino acids conserved residues at C-terminal end and a variable C-terminal end. Ongoing reports on transcriptional regulatory networks prescribe that the abscisic acid responsive element binding protein/ABRE binding factor regulon functions in ABAdependent gene expression under osmotic stress conditions (Fujita et al., 2011) and also the NAC regulon appears to be involved in osmotic stress responses (Nakashima et al., 2009). Mizoi et al. (2011) reported that the dehydration-responsive element binding protein 1 (DREB1)/C-repeat binding factor regulon functions in the cold-stress response, while the DREB2 regulon acts in heat and osmotic stress responses.

22.5.4 Gene regulatory networks A gene regulatory network explains interactions among various genes, with genes represented as nodes and their interactions as hyperlinks. These hyperlinks correspond to activation, inhibition, or suppression of the expression of a gene. This sort of network integrates all the phases of regulation of gene expression including regulation of DNA transcription, RNA translation, posttranscriptional RNA processing, and additionally the PTMs, such as protein targeting and covalent protein alteration. For the purposes of numerical modeling, the connection among interacting genes is quite often improved to activation and repression. Gene regulatory networks have been reported in a number of diverse developmental and physiological processes in plants. For instance, it has been valuable to show a gene-network-controlling stomata and guard cell closure due to abscisic acid treatment (Li et al., 2006), cell fate determination during flower development in A. thaliana (Espinosa-Soto et al., 2004), microRNA-mediated gene regulatory networks (Meng et al., 2011), and as of late in explaining the areas of plant development (Pires et al., 2013). Overall, biological network construction has been the most accepted approach in systems biology to elucidate the physiology of a living being or a biological procedure. The present-day high-throughput innovations in modern science give an enormous amount of quantitative information, though the use of quantitative data is hindered in systems wherein the knowledge of mechanistic details and kinetic parameters is rare. In such cases, an abundance of molecular data on individual constituents and interactions will be useful in modeling the system (Assmann and Albert, 2009). In spite of the limitations, these networks have given new perspectives in deciphering omics data and are connected to survey a scope of plant biological inquiries.

22.5.5 Coexpression networks Coexpression network analysis is a powerful technique to remove functional modules of coexpressed genes, explore their biological implications, and find out important novel genes. This approach distinguishes genes with diverse coexpression partners under different conditions, for example, disease states (Amar et al., 2013), tissue types (Pierson et al., 2015), and developmental stages (Xue et al., 2013), since these genes

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will probably be controllers that underlie phenotypic differences. The regulatory roles of such genes can be additionally researched by integrating data types, for example, PPIs, methylome information, interactions among TFs and their objectives, and with sequence motif study of coexpressed genes (De Smet and Marchal, 2010; Glass et al., 2013). In recent studies, worldwide coexpression networks have been developed for rice (Lee et al., 2009) and other plants (Faccioli et al., 2005; Atias et al., 2009), which have given an outline of gene gene interrelationships at the system-based level. For example, Mao et al. (2009) built an Arabidopsis gene-expression network generated from 1094 ATH1 microarrays and recognized numerous useful modules related with photosynthesis, protein biosynthesis, cell cycle, defense response, and others, and these modules discovered new bits of knowledge in gene function organization. In another coexpression study, Weston et al. (2008) have revealed how a mechanistic comprehension of adaptive physiological reactions to abiotic stress can furnish plant researchers with an apparatus of incredible prescient value in understanding species and population level adjustment to environmental change. In recent times, in silico study showed that multiple genes of different gene ontologies clustered in rice chromosomes had significant relationships with QTLs for drought-stress tolerance (Zhang et al., 2012). Also, some online resources for plant gene coexpression networks, together with CressExpress (Srinivasasainagendra et al., 2008), ATTED-II (Obayashi et al., 2009), and RiceArrayNet (Lee et al., 2009), were evolved to empower the visualization and data mining of coexpression networks for researchers. PathoPlant is probably going to be a valuable online database to analyze coregulated genes involved in plant defense reactions (Bu¨low et al., 2006). It shows signal perception and signal-transduction pathways at a molecular level during plant pathogenesis and the relating interactions amongst plants and pathogens on the organism level. A systems biology approach was likewise used to identify metabolite protein coregulation in a fundamental reaction to temperature stress in A. thaliana wildtype and a starch-deficient mutant (phosphoglucomutasedeficient) variety (Wienkoop et al., 2008). The study has additionally been utilized to recognize useful marker candidates for abiotic-stress tolerance and yield new bits of knowledge for crop improvement.

22.6 Software and algorithms for plant systems biology There are three areas that should be addressed to get full benefit of plant systems biology: (1) improvement of omics tools, (2) integration of data into usable configurations, and (3) study of data inside the area of bioinformatics. Among these, bioinformatics probably demands the maximum amount of consideration since it is fundamental that biological data be standardized and visualized to construct integrated models (Tokimatsu et al., 2005). Along these lines, all omics analysis is firmly bound with strong bioinformatics and computational tools that execute different investigation assignments yet permit integration between numerous types of data “multiomics” and empower knowledge trade between completely different organisms (Shinozaki and Sakakibara, 2009; Mochida and Shinozaki, 2011; El-Metwally et al., 2014a).

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22.6.1 Data handling and analysis The main motive, together with informatics analysis and computational devices and also related techniques and algorithms in science, is to allow biological data analysis in an exact, quick, human-error free, and effortlessly reproducible way (Orozco et al., 2013). Therefore numerous bioinformatics tasks, such as alignment of two protein or nucleotide sequences (BLAST 2 Sequences) (Tatusova and Madden, 1999), peptides and protein identification through the use of tandem MS (MS/MS) data (Perkins et al., 1999), gene prediction in eukaryotic genomic sequences (AUGUSTUS software) (Stanke and Morgenstern, 2005), genome sequence assembly (El-Metwally et al., 2013, 2014b,c), prediction of proteins’ and genes’ structural and functional features (Falda et al., 2012; Yachdav et al., 2014), prediction of PPI networks (McDowall et al., 2008; Franceschini et al., 2012), modeling of gene regulatory networks (Chaouiya et al., 2012), and some other fundamental tasks (Polpitiya et al., 2008; Henry et al., 2014), are important for plant stress multiomics analysis.

22.6.2 Visualization of plant omics data The considerable quantity of data produced by modern analytical and experimental instruments, for example, genome sequencers and mass spectrometers, and, in addition, the information resulting from the study and processing of this data requires unusual sorts of visualization. Accordingly, a few tools were developed to assist in visualizing the biological data and results in a way that would amplify the utility of the information. The reason for these data visualization tools ought to make clear, significant, and integrated resources without being blockaded by the inherent complexity of the data (Gehlenborg et al., 2010). The genome browser is a key tool that carries sequence-based data with genomic position. A few tools, for example, the genome browser, UCSC Genome Browser, and Integrated Genome Viewer (Mochida and Shinozaki, 2011; Pang et al., 2013) are accessible in different web-open resources. For instance, Gbrowse is a well-known genome program that is extensively applied on various web sites, for example, TAIR (visualizes genome annotations) (Podicheti and Dong, 2011) and Circos [visualizes genome(s) in a circular layout] (Krzywinski et al., 2009). A few proteomics data visualization tools, for example, PRIDE Inspector (visualizes and validates MS proteomics data) and ConPath (calculates orientations, orders, and gap sizes) (Kim et al., 2008; Wang et al., 2012); proteogenomics data or multiomics data visualization tools, such as OryzaPG-DB, 3Omics, Peppy (Helmy et al., 2012a; Kuo et al., 2013; Risk et al., 2013); microarray data management and data analysis tools, such as TM4 (Saeed et al., 2003), and network visualization tools, such as Cytoscape and its related web versions Cytoscape.js and Cytoscape web (Lopes et al., 2010; Ono et al., 2014), are accessible, which help in perception of “omics” data on a systems scale.

22.6.3 Storage and maintenance of data and results High output information is incredibly productive as we are able to gain additional information from it by applying various types of analyses or through combining numerous

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datasets into one big-scale comparative analysis, though this needs the data and outcomes to be moderately available and open to scientific community (Smalter Hall et al., 2013; Helmy et al., 2016). In this way, few kinds of databases are accessible online for retaining and storing the biological data and consequences (Table 22.1). The databases differ from those that keep plant records such as classification, development, production, geographical distribution (Wilkinson et al., 2012), genomic data (Yu et al., 2013; Zhao et al., 2014), transcriptomic data (Priya and Jain, 2013), proteomic data (Komatsu and Tanaka, 2005; Cheng et al., 2014), proteogenomic data (Helmy et al., 2011, 2012b), and metabolomic data (Deborde and Jacob, 2014). A few databases are unique in storing and keeping up plant stress resistance and tolerance information, for instance STIFDB2 (Arabidopsis stress responsive gene database), QlicRice, and the fungal stress response database (Smita et al., 2011; Borkotoky et al., 2013; Karanyi et al., 2013; Naika et al., 2013).

22.7 Conclusion and future prospects Plants are exposed to a variety of abiotic stresses throughout their existence on Earth. However, humans started to study abiotic stress responses and tolerance following the domestication of economically valuable plant species to maximize crop yield. Many stressful conditions cause accumulation of low-molecular weight organic compounds, compatible solutes or osmolytes, stress-specific proteins, LEA proteins, heat-shock proteins, phytochelatins, metallothioneins, and result in activation of many detoxification enzymes. Although completely different plant species have variable thresholds for stress tolerance, and a few of them can successfully tolerate severe stresses and still complete their life cycles, most cultivated crop plant species are highly sensitive and either die or suffer from productivity loss after being exposed to long periods of stress. Thus understanding and improvement of stress tolerance in crops not only present a challenging basic research problem but could also have significant impact on agricultural productivity. Although substantial efforts have been made during this direction, several research gaps need to be fulfilled. System biology approaches have given a more holistic view of the molecular response in plants once exposed to abiotic stress, and also the integration of various omics studies has revealed a new area of interactions and regulations. The integration of multiple omics technologies and coexpression interaction analysis of genes will be very helpful in accelerating abiotic-stress tolerance research in the near future. Coexpression analyses are useful in which they have revealed key regulatory hubs that can be manipulated to produce different phenotypes. The linkage of key regulatory hubs to phenotypic traits will allow for more rapid progress in the genetic manipulation and production of crop plants. Systems biology is in a developing stage and yet the future seems very bright. It offers a platform to support the global research efforts dedicated to collecting information about each and every component of a given biological system. Many strategies and technologies to have been developed integrate this information, including the semantic integration of knowledge. The role of formal mathematical and computational models in systems approaches renders the role of bioinformatics increasingly important for systems biology research. Therefore we can safely predict that systems thinking will become even more pervasive in future.

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TABLE 22.1 List of some plant specific databases and tools. Name

Description

Cereals DB

Species

URL

References

An online resource containing Wheat a range of genomic datasets (T. aestivum) for wheat (Triticum aestivum) that will assist plant breeders and scientists to select the most appropriate markers for marker-assisted selection

http://www.cerealsdb.uk.net/ CerealsDB/Documents/ DOC_CerealsDB.php

Wilkinson et al. (2012)

Bolbase

First resource platform for the B. oleracea Brassica oleracea genome and for genomic comparisons with its relatives, and thus it will help researchers to study the molecular function of genes, comparative genomics, and evolution of Brassica genomes as well as enhance molecular breeding research

http://ocri.genomics.org/bolbase Yu et al. (2013)

Bamboo GDB

A bamboo genome database with functional annotation and an analysis platform mainly based on the de novo sequencing data of moso bamboo

http://www.bamboogdb.org/

Zhao et al. (2014)

Rice SRTFDB

Oryza sativa Represents transcription of actors with comprehensive expression, cis-regulatory element, and mutant information derived from microarray data of a curated set of 456 affymetrix GeneChip rice genome arrays

http://www.nipgr.res.in/ RiceSRTFDB.html

Priya and Jain (2013)

dbPPT

A comprehensive database of protein phosphorylation in plants

Arabidopsis thaliana

http://dbppt.biocuckoo.org

Cheng et al. (2014)

P3DB 3.0

Provides more information and annotations about phosphoproteins such as gene ontology, homolog, 3D structures, kinase and phosphatase families, PPIs and protein domains, together with protein protein networks, kinase substrate or phosphatase substrate networks, and domain cooccurrence networks

A. thaliana, Medicago truncatula, and O. sativa

http://p3db.org

Yao et al. (2014)

Moso bamboo (Phyllostachys edulis)

(Continued)

Plant Life under Changing Environment

22.7 Conclusion and future prospects

TABLE 22.1

(Continued)

Name

Description

Oryza PG-DB

Rice proteome database based O. sativa on shotgun proteogenomics, contains proteome of rice undifferentiated cultured cells, corresponding cDNA, transcript and genome sequences, novel proteogenomics features, and updated gene model annotation

MeRy-B

MeRy-B is the first platform for plant 1H-NMR metabolomic profiles designed to provide a knowledge base of curated plant profiles and metabolites obtained by NMR, together with the corresponding experimental and analytical metadata

STIFDB2

QlicRice

Species

597

URL

References

http://oryzapg.iab.keio.ac.jp/

Helmy et al. (2012a,b)

Arabidopsis, O. sativa and 17 different plant species

http://bit.ly/meryb

Deborde and Jacob (2014)

A collection of biotic and abiotic stress responsive genes with options to identify probable transcription factor binding sites in their promoters. An integrated biocuration and genomic data-mining approach has been employed to characterize the data set of transcription factors and consensus binding sites from literature and stressresponsive genes from the gene expression omnibus

O. sativa ssp. japonica and Indica and Arabidopsis

http://caps.ncbs.res.in/stifdb2

Naika et al. (2013)

A collection of abiotic stress responsive QTLs in rice and their corresponding sequenced gene loci

O. sativa

http://nabg.iasri.res.in:8080/ qlic-rice

Smita et al. (2011)

PlantArrayNet Provides information on coexpressed genes using microarray-based transcriptomic data

O. sativa and two plant species

http://arraynet.mju.ac.kr/ arraynet

Lee et al. (2009)

PathoPlant

A. thaliana

http://www.pathoplant.de

Bu¨low et al. (2006)

A database on plant pathogen interactions and signal transduction on a molecular level during plant pathogenesis

(Continued)

Plant Life under Changing Environment

598

22. Abiotic-stress tolerance in plants-system biology approach

TABLE 22.1 (Continued) Name

Description

Species

URL

References

AtPID

An integrative platform for plant systems biology. It contains data relevant to PPI, protein subcellular location, ortholog maps, domain attributes, and gene regulation

A. thaliana

http://atpid.biosino.org/

Cui et al. (2007)

PODC

A repository of annotated gene expression data and omics data analysis tools

O. sativa and 7 plant species

http://bioinf.mind.meij.i.ac.jp/ podc

Ohyanagi et al. (2014)

PMRD

O. sativa and A plant miRNA data 120 plant repository containing species associated information on sequence, secondary structure, target genes, expression profiles of miRNAs, and their mapping to the species-specific genome browser

TAIR protein interaction data

TAIR curates and integrates information about genes, proteins, gene function, gene expression, mutant phenotypes, biological materials such as clones and seed stocks, genetic markers, genetic and physical maps, biochemical pathways, genome organization, images of mutant plants, and protein subcellular localizations

A. thaliana

http://www.arabidopsis.org/ submit/index.jsp

Swarbreck et al. (2007)

PRIN

PRIN is the first wellannotated protein interaction database for the important model plant O. sativa. It has greatly extended the currently available PPI data of rice with a computational approach, which will certainly provide further insights into rice functional genomics and systems biology

O. sativa

http://bis.zju.edu.cn/prin/

Gu et al. (2011)

http://bioinformatics.cau.ed.u.cn/ Zhang PMRD et al. (2010)

AtPID, A. thaliana protein interactome database; NMR, nuclear magnetic resonance; QTLs, quantitative trait loci; PMRD, plant microRNA database; PODC, Plant Omics Data Center; PPIs, protein protein interactions; STIFDB2, stress responsive transcription factor database.

Plant Life under Changing Environment

References

599

References Abbasi, F.M., Komatsu, S., 2004. A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4 (7), 2072 2081. Agarwal, P.K., Jha, B., 2010. Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol. Plant. 54 (2), 201 212. Ahuja, I., de Vos, R.C., Bones, A.M., Hall, R.D., 2010. Plant molecular stress responses face climate change. Trends Plant Sci. 15 (12), 664 674. Allwood, J.W., Goodacre, R., 2010. An introduction to liquid chromatography mass spectrometry instrumentation applied in plant metabolomic analyses. Phytochem. Anal. 21 (1), 33 47. Altelaar, A.M., Munoz, J., Heck, A.J., 2013. Next-generation proteomics: towards an integrative view of proteome dynamics. Nat. Rev. Genet. 14 (1), 35 48. Altenbach, S.B., Vensel, W.H., DuPont, F.M., 2010. Integration of transcriptomic and proteomic data from a single wheat cultivar provides new tools for understanding the roles of individual alpha gliadin proteins in flour quality and celiac disease. J. Cereal. Sci. 52 (2), 143 151. Amar, D., Safer, H., Shamir, R., 2013. Dissection of regulatory networks that are altered in disease via differential co-expression. PLoS Comput. Biol. 9 (3), e1002955. Amiour, N., Imbaud, S., Cle´ment, G., Agier, N., Zivy, M., Valot, B., et al., 2012. The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J. Exp. Bot. 63 (14), 5017 5033. Appel, R.D., Vargas, J.R., Palagi, P.M., Walther, D., Hochstrasser, D.F., 1997. Melanie II—a third-generation software package for analysis of two-dimensional electrophoresis images: II. Algorithms. Electrophoresis 18 (15), 2735 2748. Arabidopsis Interactome Mapping Consortium, 2011. Evidence for network evolution in an Arabidopsis interactome map. Science 333 (6042), 601 607. Aranda, B., Achuthan, P., Alam-Faruque, Y., Armean, I., Bridge, A., Derow, C., et al., 2009. The IntAct molecular interaction database in 2010. Nucleic Acids Res. 38, D525 D531. Assmann, S.M., Albert, R., 2009. Discrete dynamic modeling with asynchronous update, or how to model complex systems in the absence of quantitative information. Plant Systems Biology. Humana Press, pp. 207 225. Athar, H.R., Ashraf, M., 2009. Strategies for crop improvement against salinity and drought stress: an overview. Salinity and Water Stress. Springer, Dordrecht, pp. 1 16. Atias, O., Chor, B., Chamovitz, D.A., 2009. Large-scale analysis of Arabidopsis transcription reveals a basal coregulation network. BMC Syst. Biol. 3, 86. Babu, M.M., Luscombe, N.M., Aravind, L., Gerstein, M., Teichmann, S.A., 2004. Structure and evolution of transcriptional regulatory networks. Curr. Opin. Struct. Biol. 14 (3), 283 291. Ball, C.A., Awad, I.A., Demeter, J., Gollub, J., Hebert, J.M., Hernandez-Boussard, T., et al., 2005. The Stanford Microarray Database accommodates additional microarray platforms and data formats. Nucleic Acids Res. 33, D580 D582. Barkla, B.J., Vera-Estrella, R., Raymond, C., 2016. Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify saltresponsive proteins. BMC Plant Biol. 16 (1), 110. Behnke, K., Kaiser, A., Zimmer, I., Bru¨ggemann, N., Janz, D., Polle, A., et al., 2010. RNAi-mediated suppression of isoprene emission in poplar transiently impacts phenolic metabolism under high temperature and high light intensities: a transcriptomic and metabolomic analysis. Plant Mol Biol. 74 (1 2), 61 75. Blais, A., Dynlacht, B.D., 2005. Constructing transcriptional regulatory networks. Genes Dev. 19 (13), 1499 1511. Bla¨sing, O.E., Gibon, Y., Gu¨nther, M., Ho¨hne, M., Morcuende, R., Osuna, D., et al., 2005. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17 (12), 3257 3281. Blumwald, E., Grover, A., Good, A.G., 2004. Breeding for abiotic stress resistance: challenges and opportunities. In: “New Directions for a Diverse Planet”. Proceedings of the Fourth International Crop Science Congress. Brisbane, Australia. Bonhomme, L., Monclus, R., Vincent, D., Carpin, S., Lomenech, A.M., Plomion, C., et al., 2009. Leaf proteome analysis of eight Populus 3 euramericana genotypes: genetic variation in drought response and in water-use efficiency involves photosynthesis-related proteins. Proteomics 9 (17), 4121 4142.

Plant Life under Changing Environment

600

22. Abiotic-stress tolerance in plants-system biology approach

Borkotoky, S., Saravanan, V., Jaiswal, A., Das, B., Selvaraj, S., Murali, A., et al., 2013. The Arabidopsis stress responsive gene database. Int. J. Plant Genomics . Available from: https://doi.org/10.1155/2013/949564. Brooks, C., Nekrasov, V., Lippman, Z.B., Van Eck, J., 2014. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 166 (3), 1292 1297. Broughton, W.J., Hernandez, G., Blair, M., Beebe, S., Gepts, P., Vanderleyden, J., 2003. Beans (Phaseolus spp.)— model food legumes. Plant Soil 252 (1), 55 128. Buchanan, C.D., Lim, S., Salzman, R.A., Kagiampakis, I., Morishige, D.T., Weers, B.D., et al., 2005. Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol. Biol. 58 (5), 699 720. Bu¨low, L., Schindler, M., Hehl, R., 2006. PathoPlants: a platform for microarray expression data to analyze co-regulated genes involved in plant defense responses. Nucleic Acids Res. 35, D841 D845. Camejo, D., Jime´nez, A., Alarco´n, J.J., Torres, W., Go´mez, J.M., Sevilla, F., 2006. Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Funct. Plant Biol. 33 (2), 177 187. Carrari, F., Baxter, C., Usadel, B., Urbanczyk-Wochniak, E., Zanor, M.I., Nunes-Nesi, A., et al., 2006. Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol. 142 (4), 1380 1396. Cevallos-Cevallos, J.M., Reyes-De-Corcuera, J.I., Etxeberria, E., Danyluk, M.D., Rodrick, G.E., 2009. Metabolomic analysis in food science: a review. Trends Food Sci. Technol. 20 (11 12), 557 566. Chaouiya, C., Naldi, A., Thieffry, D., 2012. Logical modelling of gene regulatory networks with GINsim. Bacterial Molecular Networks. Springer, New York, pp. 463 479. Chatr-Aryamontri, A., Ceol, A., Palazzi, L.M., Nardelli, G., Schneider, M.V., Castagnoli, L., et al., 2006. MINT: the Molecular INTeraction database. Nucleic Acids Res. 35, D572 D574. Chawla, K.B.P., Kuiper, M., Bones, A.M., 2011. Systems biology: a promising tool to study abiotic stress responses. In: Tuteka, N., Gill, S.S., Tuteja, R. (Eds.), Omics and Plant Abiotic Stress Tolerance. Bentham eBooks: International Centre for Genetic Engineering and Biotechnology, New Delhi, India, pp. 163 172. Chen, L., Chen, Q., Kong, L., Xia, F., Yan, H., Zhu, Y., et al., 2016. Proteomic and physiological analysis of the response of oat (Avena sativa) seeds to heat stress under different moisture conditions. Front. Plant Sci. 7, 896. Cheng, H., Deng, W., Wang, Y., Ren, J., Liu, Z., Xue, Y., 2014. DbPPT: a comprehensive database of protein phosphorylation in plants. Database 2014, bau121. Chevreux, B., Pfisterer, T., Drescher, B., Driesel, A.J., Mu¨ller, W.E., Wetter, T., et al., 2004. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 14 (6), 1147 1159. Clarke, J.D., Zhu, T., 2006. Microarray analysis of the transcriptome as a stepping stone towards understanding biological systems: practical considerations and perspectives. Plant J. 45 (4), 630 650. Collins, N.C., Tardieu, F., Tuberosa, R., 2008. Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiol. 147 (2), 469 486. Cook, D., Fowler, S., Fiehn, O., Thomashow, M.F., 2004. A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101 (42), 15243 15248. Craigon, D.J., James, N., Okyere, J., Higgins, J., Jotham, J., May, S., 2004. NASCArrays: a repository for microarray data generated by NASC’s transcriptomics service. Nucleic Acids Res. 32, D575 D577. Cramer, G.R., Urano, K., Delrot, S., Pezzotti, M., Shinozaki, K., 2011. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 11 (1), 163. Cui, J., Li, P., Li, G., Xu, F., Zhao, C., Li, Y., et al., 2007. AtPID: Arabidopsis thaliana protein interactome database— an integrative platform for plant systems biology. Nucleic Acids Res. 36, D999 D1008. Cushman, J.C., Bohnert, H.J., 2000. Genomic approaches to plant stress tolerance. Curr. Opin. Plant Biol. 3, 117 124. De Bodt, S., Hollunder, J., Nelissen, H., Meulemeester, N., Inze´, D., 2012. CORNET 2.0: integrating plant coexpression, protein protein interactions, regulatory interactions, gene associations and functional annotations. New Phytol. 195 (3), 707 720.

Plant Life under Changing Environment

References

601

De Keersmaecker, S.C., Thijs, I., Vanderleyden, J., Marchal, K., 2006. Integration of omics data: how well does it work for bacteria? Mol. Microbiol. 62 (5), 1239 1250. De Luca, V., St Pierre, B., 2000. The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci. 5 (4), 168 173. De Smet, R., Marchal, K., 2010. Advantages and limitations of current network inference methods. Nat. Rev. Microbiol. 8 (10), 717. Deborde, C., Jacob, D., 2014. MeRy-B, a metabolomic database and knowledge base for exploring plant primary metabolism. Plant Metabolism. Humana Press, Totowa, NJ, pp. 3 16. Des Marais, D.L., Juenger, T.E., 2010. Pleiotropy, plasticity, and the evolution of plant abiotic stress tolerance. Ann. N.Y. Acad Sci. 1206 (1), 56 79. Ding, X., Richter, T., Chen, M., Fujii, H., Seo, Y.S., Xie, M., et al., 2009. A rice kinase-protein interaction map. Plant Physiol. 149 (3), 1478 1492. Dubey, R.S., 2011. Metal toxicity, oxidative stress and antioxidative defense system in plants. In: Gupta, S.D. (Ed.), Reactive Oxygen Species and Antioxidants in Higher Plants. CRC Press, Boca Raton, FL, pp. 177 203. Dubey, S., Misra, P., Dwivedi, S., Chatterjee, S., Bag, S.K., Mantri, S., et al., 2010. Transcriptomic and metabolomic shifts in rice roots in response to Cr(VI) stress. BMC Genomics 11 (1), 648. Duque, A.S., de Almeida, A.M., da Silva, A.B., da Silva, J.M., Farinha, A.P., Santos, D., et al., 2013. Abiotic stress responses in plants: unraveling the complexity of genes and networks to survive. Abiotic Stress-Plant Responses and Applications in Agriculture. InTech. Available from: https://doi.org/10.5772/52779. Edgar, R., Domrachev, M., Lash, A.E., 2002. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30 (1), 207 210. El-Metwally, S., Hamza, T., Zakaria, M., Helmy, M., 2013. Next-generation sequence assembly: four stages of data processing and computational challenges. PLoS Comput. Biol. 9 (12), e1003345. El-Metwally, S., Ouda, O.M., Helmy, M., 2014a. Next-generation sequence assembly overview. Next Generation Sequencing Technologies and Challenges in Sequence Assembly. Springer, New York, pp. 73 78. El-Metwally, S., Ouda, O.M., Helmy, M., 2014b. Next Generation Sequencing Technologies and Challenges in Sequence Assembly, Vol. 7. Springer Science & Business. El-Metwally, S., Ouda, O.M., Helmy, M., 2014c. Next-generation sequence assemblers. Next Generation Sequencing Technologies and Challenges in Sequence Assembly. Available from: http://doi.org.10.1007/9781-4939-0715-1_11. Enfissi, E.M., Barneche, F., Ahmed, I., Lichtle´, C., Gerrish, C., McQuinn, R.P., et al., 2010. Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22 (4), 1190 1215. Espinosa-Soto, C., Padilla-Longoria, P., Alvarez-Buylla, E.R., 2004. A gene regulatory network model for cell-fate determination during Arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles. Plant Cell 16 (11), 2923 2939. Faccioli, P., Provero, P., Herrmann, C., Stanca, A.M., Morcia, C., Terzi, V., 2005. From single genes to coexpression networks: extracting knowledge from barley functional genomics. Plant Mol. Biol. 58 (5), 739 750. Falda, M., Toppo, S., Pescarolo, A., Lavezzo, E., Di Camillo, B., Facchinetti, A., et al., 2012. Argot2: a large scale function prediction tool relying on semantic similarity of weighted Gene Ontology terms. BMC Bioinformatics 13 (4), S14. Available from: https://doi.org/10.1186/1471-2105-13-S4-S14. Fan, Y., Shabala, S., Ma, Y., Xu, R., Zhou, M., 2015. Using QTL mapping to investigate the relationships between abiotic stress tolerance (drought and salinity) and agronomic and physiological traits. BMC Genomics 16 (1), 43. Feller, U., Vaseva, I.I., 2014. Extreme climatic events: impacts of drought and high temperature on physiological processes in agronomically important plants. Front. Environ. Sci. 2, 39. Feng, Z., Zhang, B., Ding, W., Liu, X., Yang, D.L., Wei, P., et al., 2013. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23 (10), 1229. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., et al., 2012. STRINGv9. 1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41, D808 D815. Fujita, Y., Fujita, M., Shinozaki, K., Yamaguchi-Shinozaki, K., 2011. ABA-mediated transcriptional regulation in response to osmotic stress in plants. J. Plant Res. 124 (4), 509 525.

Plant Life under Changing Environment

602

22. Abiotic-stress tolerance in plants-system biology approach

Fukushima, A., Kusano, M., 2013. Recent progress in the development of metabolome databases for plant systems biology. Front. Plant Sci. 4, 73. Galindo Gonzalez, L.M., El Kayal, W., Ju, C.J.T., Allen, C.C., King-Jones, S., Cooke, J.E., 2012. Integrated transcriptomic and proteomic profiling of white spruce stems during the transition from active growth to dormancy. Plant Cell Environ. 35 (4), 682 701. Gao, S., Ouyang, C., Wang, S., Xu, Y., Tang, L., Chen, F., 2008. Effects of salt stress on growth, antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. seedlings. Plant Soil Environ. 54 (9), 374 381. Gao, F., Zhou, Y., Zhu, W., Li, X., Fan, L., Zhang, G., 2009. Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230 (5), 1033 1046. Garber, M., Grabherr, M.G., Guttman, M., Trapnell, C., 2011. Computational methods for transcriptome annotation and quantification using RNA-seq. Nat. Methods 8 (6), 469 477. Gehlenborg, N., O’donoghue, S.I., Baliga, N.S., Goesmann, A., Hibbs, M.A., Kitano, H., et al., 2010. Visualization of omics data for systems biology. Nat. Methods 7, S56. Gilbert, D., 2005. Biomolecular interaction network database. Brief. Bioinform. 6 (2), 194 198. Glass, K., Huttenhower, C., Quackenbush, J., Yuan, G.C., 2013. Passing messages between biological networks to refine predicted interactions. PloS One 8 (5), e64832. Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Page`s, V., Dun, E.A., Pillot, J.P., et al., 2008. Strigolactone inhibition of shoot branching. Nature 455 (7210), 189. Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., et al., 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29 (7), 644. Gu, H., Zhu, P., Jiao, Y., Meng, Y., Chen, M., 2011. PRIN: a predicted rice interactome network. BMC Bioinf. 12 (1), 161. Hajheidari, M., Eivazi, A., Buchanan, B.B., Wong, J.H., Majidi, I., Salekdeh, G.H., 2007. Proteomics uncovers a role for redox in drought tolerance in wheat. J. Proteome Res. 6 (4), 1451 1460. Hammer, G., Cooper, M., Tardieu, F., Welch, S., Walsh, B., van Eeuwijk, F., et al., 2006. Models for navigating biological complexity in breeding improved crop plants. Trends Plant Sci 11 (12), 587 593. Hashiguchi, A., Ahsan, N., Komatsu, S., 2010. Proteomics application of crops in the context of climatic changes. Food Res. Int. 43 (7), 1803 1813. Helmy, M., Tomita, M., Ishihama, Y., 2011. OryzaPG-DB: rice proteome database based on shotgun proteogenomics. BMC Plant Biol. 11 (1), 63. Helmy, M., Sugiyama, N., Tomita, M., Ishihama, Y., 2012a. The rice proteogenomics database OryzaPG-DB: development, expansion, and new features. Front. Plant Sci. 3, 65. Helmy, M., Tomita, M., Ishihama, Y., 2012b. Peptide identification by searching large-scale tandem mass spectra against large databases: bioinformatics methods in proteogenomics. Genes Genome Genomics 6, 76 85. Helmy, M., Crits-Christoph, A., Bader, G.D., 2016. Ten simple rules for developing public biological databases. PLoS Comput. Biol. 12 (11), e1005128. Henry, V.J., Bandrowski, A.E., Pepin, A.S., Gonzalez, B.J., Desfeux, A., 2014. OMICtools: an informative directory for multi-omic data analysis. Database 2014. Avaliable from: https://doi.org/10.1093/database/bau069. Herna´ndez, G., Ramı´rez, M., Valde´s-Lo´pez, O., Tesfaye, M., Graham, M.A., Czechowski, T., et al., 2007. Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol. 144 (2), 752 767. Hirai, M.Y., Yano, M., Goodenowe, D.B., Kanaya, S., Kimura, T., Awazuhara, M., et al., 2004. Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 101 (27), 10205 10210. Hoefgen, R., Nikiforova, V.J., 2008. Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol. Plant. 132 (2), 190 198. Hoogland, C., Sanchez, J.C., Tonella, L., Binz, P.A., Bairoch, A., Hochstrasser, D.F., et al., 2000. The 1999 SWISS2DPAGE database update. Nucleic Acids Res. 28 (1), 286 288. Houle, D., Govindaraju, D.R., Omholt, S., 2010. Phenomics: the next challenge. Nat. Rev. Genet. 11 (12), 855. Hu, H., Dai, M., Yao, J., Xiao, B., Li, X., Zhang, Q., et al., 2006. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. U.S.A. 103 (35), 12987 12992. Huang, X., Madan, A., 1999. CAP3: a DNA sequence assembly program. Genome Res. 9 (9), 868 877.

Plant Life under Changing Environment

References

603

Huang, J., Sun, S.J., Xu, D.Q., Yang, X., Bao, Y.M., Wang, Z.F., et al., 2009. Increased tolerance of rice to cold, drought and oxidative stresses mediated by the overexpression of a gene that encodes the zinc finger protein ZFP245. Biochem. Biophys. Res. Commun. 389 (3), 556 561. Izawa, T., Mihara, M., Suzuki, Y., Gupta, M., Itoh, H., Nagano, A.J., et al., 2011. Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. Plant Cell 23 (5), 1741 1755. Jaleel, C.A., Gopi, R., Panneerselvam, R., 2008. Growth and photosynthetic pigments responses of two varieties of Catharanthus roseus to triadimefon treatment. C.R. Biol. 331 (4), 272 277. Jogaiah, S., Govind, S.R., Tran, L.S.P., 2013. Systems biology-based approaches toward understanding drought tolerance in food crops. Crit. Rev. Biotechnol. 33 (1), 23 39. Joosen, R.V., Ligterink, W., Dekkers, B.J., Hilhorst, H.W., 2011. Visualization of molecular processes associated with seed dormancy and germination using MapMan. Seed Sci. Res. 21 (2), 143 152. Joung, J.G., Corbett, A.M., Fellman, S.M., Tieman, D.M., Klee, H.J., Giovannoni, J.J., et al., 2009. Plant MetGenMAP: an integrative analysis system for plant systems biology. Plant Physiol. 151 (4), 1758 1768. Kim, P.G., Cho, H.G., Park, K., 2008. A scaffold analysis tool using mate-pair information in genome sequencing. J. Biomed. Biotechnol. 2008, 675741. Available from: https://doi.org/10.1155/2008/675741. Kim, H.K., Choi, Y.H., Verpoorte, R., 2011. NMR-based plant metabolomics: where do we stand, where do we go? Trends Biotechnol. 29 (6), 267 275. Kitano, H., 2002. Systems biology: a brief overview. Science 295 (5560), 1662 1664. Karanyi, Z., Holb, I., Hornok, L., Pocsi, I., Miskei, M., 2013. FSRD: fungal stress response database. Database 2013, bat037. Kempa, S., Krasensky, J., Dal Santo, S., Kopka, J., Jonak, C., 2008. A central role of abscisic acid in stress-regulated carbohydrate metabolism. PloS One 3 (12), e3935. Kerrien, S., Alam-Faruque, Y., Aranda, B., Bancarz, I., Bridge, A., Derow, C., et al., 2006. IntAct—open source resource for molecular interaction data. Nucleic Acids Res. 35, D561 D565. Kiemer, L., Cesareni, G., 2007. Comparative interactomics: comparing apples and pears? Trends Biotechnol. 25 (10), 448 454. Kogel, K.H., Voll, L.M., Scha¨fer, P., Jansen, C., Wu, Y., Langen, G., et al., 2010. Transcriptome and metabolome profiling of field-grown transgenic barley lack induced differences but show cultivar-specific variances. Proc. Natl. Acad. Sci. U.S.A. 107 (14), 6198 6203. Komatsu, S., Hossain, Z., 2013. Organ-specific proteome analysis for identification of abiotic stress response mechanism in crop. Front. Plant Sci. 4, 71. Komatsu, S., Tanaka, N., 2005. Rice proteome analysis: a step toward functional analysis of the rice genome. Proteomics 5 (4), 938 949. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., et al., 2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19 (9), 1639 1645. Kumar, V., Jain, M., 2014. The CRISPR Cas system for plant genome editing: advances and opportunities. J. Exp. Bot. 66 (1), 47 57. Kuo, T.C., Tian, T.F., Tseng, Y.J., 2013. 3Omics: a web-based systems biology tool for analysis, integration and visualization of human transcriptomic, proteomic and metabolomic data. BMC Syst. Biol. 7 (1), 64. Le, D.T., Nishiyama, R., Watanabe, Y., Tanaka, M., Seki, M., Yamaguchi-Shinozaki, K., et al., 2012. Differential gene expression in soybean leaf tissues at late developmental stages under drought stress revealed by genome-wide transcriptome analysis. PLoS One 7 (11), e49522. Lee, T.H., Kim, Y.K., Pham, T.T.M., Song, S.I., Kim, J.K., Kang, K.Y., et al., 2009. RiceArrayNet: a database for correlating gene expression from transcriptome profiling, and its application to the analysis of coexpressed genes in rice. Plant Physiol. 151 (1), 16 33. Li, S., Assmann, S.M., Albert, R., 2006. Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol. 4 (10), e312. Licata, L., Briganti, L., Peluso, D., Perfetto, L., Iannuccelli, M., Galeota, E., et al., 2011. MINT, the molecular interaction database: 2012 update. Nucleic Acids Res. 40, D857 D861. Lin, M., Zhou, X., Shen, X., Mao, C., Chen, X., 2011. The predicted Arabidopsis interactome resource and network topology-based systems biology analyses. Plant Cell 23 (3), 911 922. Lopes, C.T., Franz, M., Kazi, F., Donaldson, S.L., Morris, Q., Bader, G.D., 2010. Cytoscape Web: an interactive web-based network browser. Bioinformatics 26 (18), 2347 2348.

Plant Life under Changing Environment

604

22. Abiotic-stress tolerance in plants-system biology approach

Luo, Z.B., Janz, D., Jiang, X., Goebel, C., Wildhagen, H., Tan, Y., et al., 2009. Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol. 151 (4), 1902 1917. Luo, M., Liu, J., Lee, R.D., Scully, B.T., Guo, B., 2010. Monitoring the expression of maize genes in developing kernels under drought stress using oligo-microarray. J. Integr. Plant Biol. 52 (12), 1059 1074. Maheshwari, R., Dubey, R.S., 2007. Nickel toxicity inhibits ribonuclease and protease activities in rice seedlings: protective effects of proline. Plant Growth Regul. 51, 231 243. Mao, L., van Hemert, J.L., Dash, S., Dickerson, J.A., 2009. Arabidopsis gene co-expression network and its functional modules. BMC Bioinf. 10 (1), 346. Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L., Suzuki, A., 2010. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann. Bot. 105 (7), 1141 1157. Mathur, S., Jajoo, A., 2014. Effects of heat stress on growth and crop yield of wheat (Triticum aestivum). Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment. Springer, New York, pp. 163 191. McDowall, M.D., Scott, M.S., Barton, G.J., 2008. PIPs: human protein protein interaction prediction database. Nucleic Acids Res. 37, D651 D656. Meng, Y., Shao, C., Chen, M., 2011. Toward microRNA-mediated gene regulatory networks in plants. Brief. Bioinform. 12 (6), 645 659. Metzker, M.L., 2010. Sequencing technologies—the next generation. Nat. Rev. Genet. 11 (1), 31. Mishra, S., Dubey, R.S., 2008. Changes in phosphate content and phosphatase activities in rice seedlings exposed to arsenite. Braz. J. Plant Physiol. 20, 19 28. Mishra, P., Bhoomika, K., Dubey, R.S., 2013. Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma 250 (1), 3 19. Mizoi, J., Shinozaki, K., Yamaguchi-Shinozaki, K., 2011. AP2/ERF family transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 5, 86 96. Mochida, K., Shinozaki, K., 2010. Genomics and bioinformatics resources for crop improvement. Plant Cell Physiol. 51 (4), 497 523. Mochida, K., Shinozaki, K., 2011. Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant Cell Physiol. 52 (12), 2017 2038. Moreno-Risueno, M.A., Busch, W., Benfey, P.N., 2010. Omics meet networks—using systems approaches to infer regulatory networks in plants. Curr. Opin. Plant Biol. 13 (2), 126 131. Morsy, M., Gouthu, S., Orchard, S., Thorneycroft, D., Harper, J.F., Mittler, R., et al., 2008. Charting plant interactomes: possibilities and challenges. Trends Plant Sci. 13 (4), 183 191. Mostafavi, S., Ray, D., Warde-Farley, D., Grouios, C., Morris, Q., 2008. GeneMANIA: a real-time multiple association network integration algorithm for predicting gene function. Genome Biol. 9 (1), S4. Mukhtar, M.S., Carvunis, A.R., Dreze, M., Epple, P., Steinbrenner, J., Moore, J., et al., 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333 (6042), 596 601. Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651 681. Nachappa, P., Levy, J., Tamborindeguy, C., 2012. Transcriptome analyses of Bactericera cockerelli adults in response to “Candidatus Liberibacter solanacearum” infection. Mol. Genet. Genomics 287 (10), 803 817. Naika, M., Shameer, K., Mathew, O.K., Gowda, R., Sowdhamini, R., 2013. STIFDB2: an updated version of plant stress-responsive transcription factor database with additional stress signals, stress-responsive transcription factor binding sites and stress-responsive genes in Arabidopsis and rice. Plant Cell Physiol. 54 (2), e8. Nakashima, K., Ito, Y., Yamaguchi-Shinozaki, K., 2009. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 149 (1), 88 95. Nikiforova, V.J., Daub, C.O., Hesse, H., Willmitzer, L., Hoefgen, R., 2005. Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J. Exp. Bot 56 (417), 1887 1896. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., Kinoshita, K., 2009. ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37, D987 D991. Ohyanagi, H., Takano, T., Terashima, S., Kobayashi, M., Kanno, M., Morimoto, K., et al., 2014. Plant Omics Data Center: an integrated web repository for interspecies gene expression networks with NLP-based curation. Plant Cell Physiol. 56 (1), e9.

Plant Life under Changing Environment

References

605

Ono, K., Demchak, B., Ideker, T., 2014. Cytoscape tools for the web age: D3.js and Cytoscape.js exporters. F1000 Research 3, 143. Orozco, A., Morera, J., Jime´nez, S., Boza, R., 2013. A review of bioinformatics training applied to research in molecular medicine, agriculture and biodiversity in Costa Rica and Central America. Briefings Bioinf. 14 (5), 661 670. Osakabe, Y., Osakabe, K., Shinozaki, K., Tran, L.S.P., 2014. Response of plants to water stress. Front. Plant Sci. 5, 86. Palaniswamy, S.K., James, S., Sun, H., Lamb, R.S., Davuluri, R.V., Grotewold, E., 2006. AGRIS and AtRegNet. a platform to link cis-regulatory elements and transcription factors into regulatory networks. Plant Physiol. 140 (3), 818 829. Pang, C.N.I., Tay, A.P., Aya, C., Twine, N.A., Harkness, L., Hart-Smith, G., et al., 2013. Tools to covisualize and coanalyze proteomic data with genomes and transcriptomes: validation of genes and alternative mRNA splicing. J. Proteome Res. 13 (1), 84 98. Parkinson, H., Sarkans, U., Shojatalab, M., Abeygunawardena, N., Contrino, S., Coulson, R., et al., 2005. ArrayExpress—a public repository for microarray gene expression data at the EBI. Nucleic Acids Res. 33, D553 D555. Peng, H., Geng, W., Yong-Quan, W., Mao-Teng, L., Jun, X., Long-Jiang, Y., 2010. Effect of heavy metal stress on emerging plants community constructions in wetland. Water Sci. Technol. 62 (10), 2459 2466. Perkins, D.N., Pappin, D.J., Creasy, D.M., Cottrell, J.S., 1999. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20 (18), 3551 3567. Peyraud, R., Dubiella, U., Barbacci, A., Genin, S., Raffaele, S., Roby, D., 2017. Advances on plant pathogen interactions from molecular toward systems biology perspectives. Plant J. 90 (4), 720 737. Pichersky, E., Gang, D.R., 2000. Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends Plant Sci. 5 (10), 439 445. Pierson, E., Koller, D., Battle, A., Mostafavi, S., GTEx Consortium, 2015. Sharing and specificity of co-expression networks across 35 human tissues. PLoS Comput. Biol. 11 (5), e1004220. Pires, N.D., Yi, K., Breuninger, H., Catarino, B., Menand, B., Dolan, L., 2013. Recruitment and remodeling of an ancient gene regulatory network during land plant evolution. Proc. Natl. Acad. Sci. U.S.A. 110 (23), 9571 9576. Podicheti, R., Dong, Q., 2011. Administering GBrowse sites with WebGBrowse. Curr. Protoc. Bioinf. Chapter 9: Unit 9.14. Avaliable from: https://doi.org/10.1002/0471250953.bi0914s33. Polpitiya, A.D., Qian, W.J., Jaitly, N., Petyuk, V.A., Adkins, J.N., Camp, D.G., et al., 2008. DAnTE: a statistical tool for quantitative analysis of -omics data. Bioinformatics 24 (13), 1556 1558. Priya, P., Jain, M., 2013. RiceSRTFDB: a database of rice transcription factors containing comprehensive expression, cis-regulatory element and mutant information to facilitate gene function analysis. Database 2013, bat027. Proietti, S., Bertini, L., Timperio, A.M., Zolla, L., Caporale, C., Caruso, C., 2013. Crosstalk between salicylic acid and jasmonate in Arabidopsis investigated by an integrated proteomic and transcriptomic approach. Mol. Biosyst. 9 (6), 1169 1187. Rischer, H., Oreˇsiˇc, M., Seppa¨nen-Laakso, T., Katajamaa, M., Lammertyn, F., Ardiles-Diaz, W., et al., 2006. Geneto-metabolite networks for terpenoid indole alkaloid biosynthesis in Catharanthus roseus cells. Proc. Natl. Acad. Sci. U.S.A. 103 (14), 5614 5619. Risk, B.A., Spitzer, W.J., Giddings, M.C., 2013. Peppy: proteogenomic search software. J. Proteome Res. 12 (6), 3019 3025. Rodziewicz, P., Swarcewicz, B., Chmielewska, K., Wojakowska, A., Stobiecki, M., 2014. Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol. Plant. 36 (1), 1 19. Rosengren, A.T., Salmi, J.M., Aittokallio, T., Westerholm, J., Lahesmaa, R., Nyman, T.A., et al., 2003. Comparison of PDQuest and Progenesis software packages in the analysis of two-dimensional electrophoresis gels. Proteomics 3 (10), 1936 1946. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., et al., 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34 (2), 374. Saito, K., Matsuda, F., 2010. Metabolomics for functional genomics, systems biology, and biotechnology. Annu. Rev. Plant Biol. 61, 463 489. Salwinski, L., Miller, C.S., Smith, A.J., Pettit, F.K., Bowie, J.U., Eisenberg, D., 2004. The database of interacting proteins: 2004 update. Nucleic Acids Res. 32, D449 D451.

Plant Life under Changing Environment

606

22. Abiotic-stress tolerance in plants-system biology approach

Sauer, U., Heinemann, M., Zamboni, N., 2007. Getting closer to the whole picture. Science (Washington) 316 (5824), 550 551. Schutzendubel, A., Polle, A., 2002. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot 53 (372), 1351 1365. Sharan, R., Ideker, T., 2006. Modeling cellular machinery through biological network comparison. Nat. Biotechnol. 24 (4), 427. Sharma, P., Dubey, R.S., 2007. Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep. 26, 2027 2038. Sharma, S.S., Dietz, K.J., 2009. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 14 (1), 43 50. Shen, H., Liu, C., Zhang, Y., Meng, X., Zhou, X., Chu, C., et al., 2012. OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol. Biol. 80 (3), 241 253. Sheth, B.P., Thaker, V.S., 2014. Plant systems biology: insights, advances and challenges. Planta 240 (1), 33 54. Shingaki-Wells, R.N., Huang, S., Taylor, N.L., Carroll, A.J., Zhou, W., Millar, A.H., 2011. Differential molecular responses of rice and wheat coleoptiles to anoxia reveal novel metabolic adaptations in amino acid metabolism for tissue tolerance. Plant Physiol. 156 (4), 1706 1724. Shinozaki, K., Sakakibara, H., 2009. Omics and bioinformatics: an essential toolbox for systems analyses of plant functions beyond 2010. Plant Cell Physiol. 50, 1177 1180. Sicher, R.C., Barnaby, J.Y., 2012. Impact of carbon dioxide enrichment on the responses of maize leaf transcripts and metabolites to water stress. Physiol. Plant. 144 (3), 238 253. Skylas, D.J., Cordwell, S.J., Hains, P.G., Larsen, M.R., Basseal, D.J., Walsh, B.J., et al., 2002. Heat shock of wheat during grain filling: proteins associated with heat-tolerance. J. Cereal Sci. 35 (2), 175 188. Smalter Hall, A., Shan, Y., Lushington, G., Visvanathan, M., 2013. An overview of computational life science databases & exchange formats of relevance to chemical biology research. Comb. Chem. High Throughput Screen. 16 (3), 189 198. Smita, S., Lenka, S.K., Katiyar, A., Jaiswal, P., Preece, J., Bansal, K.C., 2011. QlicRice: a web interface for abiotic stress responsive QTL and loci interaction channels in rice. Database 2011, bar037. Srinivasasainagendra, V., Page, G.P., Mehta, T., Coulibaly, I., Loraine, A.E., 2008. CressExpress: a tool for largescale mining of expression data from Arabidopsis. Plant Physiol. 147, 1004 1016. Srivastava, S., Dubey, R.S., 2011. Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul. 64, 1 16. Srivastava, V., Obudulu, O., Bygdell, J., Lo¨fstedt, T., Ryde´n, P., Nilsson, R., et al., 2013. OnPLS integration of transcriptomic, proteomic and metabolomic data shows multi-level oxidative stress responses in the cambium of transgenic hipI-superoxide dismutase Populus plants. BMC Genomics 14 (1), 893. Stanke, M., Morgenstern, B., 2005. AUGUSTUS: a web server for gene prediction in eukaryotes that allows userdefined constraints. Nucleic Acids Res. 33, W465 W467. Stark, C., Breitkreutz, B.J., Reguly, T., Boucher, L., Breitkreutz, A., Tyers, M., 2006. BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34, D535 D539. Steinfath, M., Repsilber, D., Scholz, M., Walther, D., Selbig, J., 2007. Integrated data analysis for genome-wide research. EXS 97, 309 329. Swarbreck, D., Wilks, C., Lamesch, P., Berardini, T.Z., Garcia-Hernandez, M., Foerster, H., et al., 2007. The Arabidopsis information resource (TAIR): gene structure and function annotation. Nucleic Acids Res. 36, D1009 D1014. Tabata, S., 2002. Impact of genomics approaches on plant genetics and physiology. J. Plant Res. 115 (4), 271 275. Talame, V., Ozturk, N.Z., Bohnert, H.J., Tuberosa, R., 2007. Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J. Exp. Bot. 5, 229 240. Tardif, G., Kane, N.A., Adam, H., Labrie, L., Major, G., Gulick, P., et al., 2007. Interaction network of proteins associated with abiotic stress response and development in wheat. Plant Mol. Biol. 63 (5), 703 718. Tatusova, T.A., Madden, T.L., 1999. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174 (2), 247 250. Tester, M., Langridge, P., 2010. Breeding technologies to increase crop production in a changing world. Science 327 (5967), 818 822.

Plant Life under Changing Environment

References

607

Tokimatsu, T., Sakurai, N., Suzuki, H., Ohta, H., Nishitani, K., Koyama, T., et al., 2005. KaPPA-View. A webbased analysis tool for integration of transcript and metabolite data on plant metabolic pathway maps. Plant Physiol. 138 (3), 1289 1300. Trewavas, A., 2006. A brief history of systems biology: “Every object that biology studies is a system of systems.” Francois Jacob (1974). Plant Cell 18 (10), 2420 2430. Turenne, N., 2011. Role of a web-based software platform for systems biology. J. Comput. Sci. Syst. Biol. 4, 035 041. Uhrig, J.F., 2006. Protein interaction networks in plants. Planta 224 (4), 771 781. Umezawa, T., Fujita, M., Fujita, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., 2006. Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr. Opin. Biotechnol. 17 (2), 113 122. Urano, K., Kurihara, Y., Seki, M., Shinozaki, K., 2010. ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr. Opin. Plant Biol. 13 (2), 132 138. Urbanczyk-Wochniak, E., Usadel, B., Thimm, O., Nunes-Nesi, A., Carrari, F., Davy, M., et al., 2006. Conversion of MapMan to allow the analysis of transcript data from Solanaceous species: effects of genetic and environmental alterations in energy metabolism in the leaf. Plant Mol. Biol. 60 (5), 773 792. VanBogelen, R.A., Schiller, E.E., Thomas, J.D., Neidhardt, F.C., 1999. Diagnosis of cellular states of microbial organisms using proteomics. Electrophoresis 20 (11), 2149 2159. Vernoux, T., Brunoud, G., Farcot, E., Morin, V., Van den Daele, H., Legrand, J., et al., 2011. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol. Syst. Biol. 7 (1), 508. Vihinen, M., 2001. Bioinformatics in proteomics. Biomol. Eng. 18 (5), 241 248. ˇ ´ , V., Opatrna´, J., Ahmed, J., 2007. WCS120 protein family and proVı´ta´mva´s, P., Saalbach, G., Pra´sˇ il, I.T., Capkova teins soluble upon boiling in cold-acclimated winter wheat. J. Plant Physiol. 164 (9), 1197 1207. Voytas, D.F., 2013. Plant genome engineering with sequence-specific nucleases. Annu. Rev. Plant. Biol. 64, 327 350. Wakasa, Y., Oono, Y., Yazawa, T., Hayashi, S., Ozawa, K., Handa, H., et al., 2014. RNA sequencing-mediated transcriptome analysis of rice plants in endoplasmic reticulum stress conditions. BMC Plant Biol 14 (1), 101. Available from: https://doi.org/10.1186/1471-2229-14-101. Wang, L., Li, P., Brutnell, T.P., 2010. Exploring plant transcriptomes using ultra high-throughput sequencing. Brief. Funct. Genomics 9 (2), 118 128. Wang, R., Fabregat, A., Rı´os, D., Ovelleiro, D., Foster, J.M., Coˆte´, et al., 2012. PRIDE Inspector: a tool to visualize and validate MS proteomics data. Nat. Biotech 30 (2), 135 137. Wang, H., Schauer, N., Usadel, B., Frasse, P., Zouine, M., Hernould, M., et al., 2009a. Regulatory features underlying pollination-dependent and-independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21 (5), 1428 1452. Wang, L., Feng, Z., Wang, X., Wang, X., Zhang, X., 2009b. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26 (1), 136 138. Wang, C.Y., Shen, R.F., Wang, C., Wang, W., 2013. Root protein profile changes induced by Al exposure in two rice cultivars differing in Al tolerance. J. Proteomics 78, 281 293. Weckwerth, W., Kahl, G. (Eds.), 2013. The Handbook of Plant Metabolomics. John Wiley & Sons. Weston, D.J., Gunter, L.E., Rogers, A., Wullschleger, S.D., 2008. Connecting genes, coexpression modules, and molecular signatures to environmental stress phenotypes in plants. BMC. Syst. Biol. 2 (1), 16. Wienkoop, S., Morgenthal, K., Wolschin, F., Scholz, M., Selbig, J., Weckwerth, W., 2008. Integration of metabolomic and proteomic phenotypes analysis of data covariance dissects starch and RFO metabolism from low and high temperature compensation response in Arabidopsis thaliana. Mol. Cell. Proteomics 7 (9), 1725 1736. Wilkinson, P.A., Winfield, M.O., Barker, G.L., Allen, A.M., Burridge, A., Coghill, J.A., et al., 2012. CerealsDB 2.0: an integrated resource for plant breeders and scientists. BMC Bioinf. 13 (1), 219. Wishart, D.S., 2008. Metabolomics: applications to food science and nutrition research. Trends Food Sci. Technol. 19 (9), 482 493. Wu, L.B., Shhadi, M.Y., Gregorio, G., Matthus, E., Becker, M., Frei, M., 2014. Genetic and physiological analysis of tolerance to acute iron toxicity in rice. Rice 7 (1), 8. Xiao, B., Huang, Y., Tang, N., Xiong, L., 2007. Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor. Appl. Genet. 115 (1), 35 46. Xue, Z., Huang, K., Cai, C., Cai, L., Jiang, C.Y., Feng, Y., et al., 2013. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500 (7464), 593.

Plant Life under Changing Environment

608

22. Abiotic-stress tolerance in plants-system biology approach

Yachdav, G., Kloppmann, E., Kajan, L., Hecht, M., Goldberg, T., Hamp, T., et al., 2014. PredictProtein—an open resource for online prediction of protein structural and functional features. Nucleic Acids Res 42 (W1), W337 W343. Yamakawa, H., Hakata, M., 2010. Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant Cell Physiol. 51 (5), 795 809. Yao, Q., Ge, H., Wu, S., Zhang, N., Chen, W., Xu, C., et al., 2014. P3DB 3.0: from plant phosphorylation sites to protein networks. Nucleic Acids Res. 42 (D1), D1206 D1213. Yin, X., Chasalow, S.D., Dourleijn, C.J., Stam, P., Kropff, M.J., 2000. Coupling estimated effects of QTLs for physiological traits to a crop growth model: predicting yield variation among recombinant inbred lines in barley. Heredity 85 (6), 539 549. Yin, C.C., Ma, B., Collinge, D.P., Pogson, B.J., He, S.J., Xiong, Q., et al., 2015. Ethylene responses in rice roots and coleoptiles are differentially regulated by a carotenoid isomerase-mediated abscisic acid pathway. Plant Cell 27 (4), 1061 1081. Yin, X., Struik, P.C., Kropff, M.J., 2004. Role of crop physiology in predicting gene-to-phenotype relationships. Trends Plant Sci 9 (9), 426 432. Yu, L.J., Luo, Y.F., Liao, B., Xie, L.J., Chen, L., Xiao, S., et al., 2012. Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryza sativa). New Phytol. 195 (1), 97 112. Yu, J., Zhao, M., Wang, X., Tong, C., Huang, S., Tehrim, S., et al., 2013. Bolbase: a comprehensive genomics database for Brassica oleracea. BMC Genomics 14 (1), 664. Yuan, J.S., Galbraith, D.W., Dai, S.Y., Griffin, P., Stewart Jr, C.N., 2008. Plant systems biology comes of age. Trends Plant Sci. 13 (4), 165 171. Zerbino, D.R., Birney, E., 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18 (5), 821 829. Zhang, Y., Gao, P., Yuan, J.S., 2010. Plant protein-protein interaction network and interactome. Curr. Genomics 11 (1), 40 46. Zhang, L., Yu, S., Zuo, K., Luo, L., Tang, K., 2012. Identification of gene modules associated with drought response in rice by network-based analysis. PLoS One 7 (5), e33748. Zhang, H., Zhang, J., Wei, P., Zhang, B., Gou, F., Feng, Z., et al., 2014a. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol. J. 12 (6), 797 807. Zhang, Y., Cheng, Y., Guo, J., Yang, E., Liu, C., Zheng, X., et al., 2014b. Comparative transcriptome analysis to reveal genes involved in wheat hybrid necrosis. Int. J. Mol. Sci. 15 (12), 23332 23344. Zhao, H., Peng, Z., Fei, B., Li, L., Hu, T., Gao, Z., et al., 2014. BambooGDB: a bamboo genome database with functional annotation and an analysis platform. Database 2014, bau006. Zhu, Y.N., Shi, D.Q., Ruan, M.B., Zhang, L.L., Meng, Z.H., Liu, J., et al., 2013. Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic stresses in cotton (Gossypium hirsutum L.). PloS One 8 (11), e80218. Zimmermann, I.M., Heim, M.A., Weisshaar, B., Uhrig, J.F., 2004. Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J. 40 (1), 22 34. Zulak, K.G., Cornish, A., Daskalchuk, T.E., Deyholos, M.K., Goodenowe, D.B., Gordon, P.M., et al., 2007. Gene transcript and metabolite profiling of elicitor-induced opium poppy cell cultures reveals the coordinate regulation of primary and secondary metabolism. Planta 225 (5), 1085 1106.

Further reading Baum, B., Craig, G., 2004. RNAi in a postmodern, postgenomic era. Oncogene 23 (51), 8336 8339. Cruz, L.M., Trefflich, S., Weiss, V.A., Castro, M.A.A., 2017. Protein function prediction. Functional Genomics. Humana Press, New York, pp. 55 75. Geisberg, J.V., Struhl, K., 2004. Quantitative sequential chromatin immunoprecipitation, a method for analyzing co-occupancy of proteins at genomic regions in vivo. Nucleic Acids Res. 32 (19), e151. Nachman, I., Regev, A., Friedman, N., 2004. Inferring quantitative models of regulatory networks from expression data. Bioinformatics 20 (1), i248 i256.

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Perez-Riverol, Y., Xu, Q.W., Wang, R., Uszkoreit, J., Griss, J., Sanchez, A., et al., 2016. PRIDE Inspector Toolsuite: moving toward a universal visualization tool for proteomics data standard formats and quality assessment of ProteomeXchange datasets. Mol. Cell. Proteomics 15 (1), 305 317. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., et al., 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13 (11), 2498 2504.

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C H A P T E R

23 Plant single-cell biology and abiotic stress tolerance Mohsin Tanveer1 and Urwa Yousaf2 1

School of Land and Food, University of Tasmania, Hobart, Australia 2Department of Computer Sciences, University of Agriculture Faisalabad, Faisalabad, Pakistan

23.1 Introduction Plant single-cell biology aims to understand complex biological processes in plant cells. It is imperative to study numerous physiological and transcriptional responses in cells under abiotic stresses. In current situation of climate change, plant scientists are trying to gain new insights in cellular responses under abiotic stress conditions. This chapter describes the scope of plant single-cell biology and different single-cell models. We also highlight the role of computational biology in studying plant single-cell biology and abiotic stress tolerance.

23.1.1 Need of plant single-cell biology approach Abiotic stresses, such as drought, salt, waterlogging, share numerous similar mechanisms to reduce plant productivity, such as reduced carbon fixation, oxidation, and others (Tanveer et al., 2018; Hussain et al., 2018a,b). Although different studies documented differential plant responses to single or combined stresses, understanding of abiotic stress tolerance mechanisms is not yet cleared. Plant single-cell biology aims to explain and underpin complex biological responses via the integration of different data sets at cell level (Alberts et al., 2013). This field of study further reveals numerous biochemical and molecular processes in cells, which is why it is also called plant single-cell systematic biology. During the last few decades, different strategies have been used to study plant biology at tissue, organ, or whole plant level by analyzing biological activities and responses of different plant tissues and organs to abiotic stress tolerance. This results in the characterization of the functions of different genes in response to different abiotic stresses. Contrarily, these approaches show dilution effect because of homogeneity of tissues or organs.

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Simpson (1951) and Yule (1902) documented a concept called the Yule Simpson paradox. According to this concept, distinct properties of individual plant cells cannot be differentiated while examining complex structures (tissues or organs) (Libault et al., 2017). Furthermore, low-abundant organic molecules are also problematic to examine and differentiate from complex biological structures.

23.2 Single-cell models In animals, single cell type analysis has been widely carried out to study complex biological mechanisms in cells (Gawad et al., 2016). However, in plants, such studies are difficult due to complex genetic makeup and plant’s differential responses to stress environment at plant single-cell level. Nonetheless, with time, developments progressed, and new plant single cell and single cell type models have emerged to gain insight into abiotic stress responses in plants. Several studies employed cotton fibers, trichomes, root hairs, guard cells, and pollens as single-cell types to study abiotic stress effects and responses (Jin et al., 2013; Yang and Ye, 2013; Rutley and Twell, 2015; Wang et al., 2016a,b). Each of these cell types possesses unique physiological and biological characteristics that help in separating them from the rest of the plant (Becker et al., 2003; Arpat et al., 2004; Marks et al., 2008; Qiao and Libault, 2013).

23.2.1 Male and female gametophytes Numerous single cell type models are presently used in different studies depending on their key biological roles in plant growth and development. For instance, male gametophytic cells in plants are being used to analyze plant cell polar expansion and pre- and postfertilization events (McCormick, 2013). Similarly, female gametophyte (comprising single egg cell, two synergid, or three antipodal cells) is also an important model while studying the effects of different abiotic stresses at plant cell level. Female gametophyte allows the study of cell polarity, meiosis and mitosis processes, and function of plant gametes (Russell, 1992; Wuest et al., 2010; Hamamura et al., 2011). These models help in understanding the detrimental effects of abiotic stress and plant defense mechanism at plant cell levels.

23.2.2 Guard cells Guard cells are another type of plant single-cell models to study early signal transduction and stress tolerance mechanisms in plants. Guard cells are surrounded by stomatal pores and are located in leaf epidermis. Guard cells control influx and efflux of CO2 and water from leaves, respectively. Studies showed differential guard cell responses under different abiotic stresses (Irving et al., 1992; Luan, 2002; Chaves et al., 2003; Garcia-Mata et al., 2003; Geiger et al., 2009). Studies on guard cells show better understanding of signaling network in guard cells. Guard cells are very useful single-cell models, which can help

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to differentiate the role of different genes and proteins in stress signaling networks. Studies based on engineering stomatal guard cell can provide major contribution to develop stress tolerant plants.

23.2.3 Trichomes Trichomes, which originated from the epidermal cells, are very specialized structures and play very key role in different plant processes. Trichomes have been considered a model system to study single-cell biology and cell differentiation and endo-reduplication (Schellmann and Hu¨lskamp, 2005). Key roles of trichomes in plant physiology include carbon assimilation, turgor maintenance via modulating leaf water loss, and mechanical and chemical defense systems (Wagner, 1991; Wagner et al., 2004). Several studies have also indicated that trichomes are major sites of biosynthesis of secondary metabolites and stress proteins (Aziz et al., 2005; Shepherd et al., 2005; Bertea et al., 2006; Kroumova et al., 2007; Nagel et al., 2008). Trichomes help plants in stress adaptation by developing glutathione and sulfur-dependent defense mechanism and by redox regulation. Gutierre´z-Alcala´ et al. (2000) and Wienkoop et al. (2004) observed high expression levels of different genes encoding for sulfur assimilation and other stress proteins such as glutathione (GSH). Similar results also have been reported in the trichomes of tobacco; thus trichomes are very important single-cell models (Amme et al., 2005). Cotton fibers are another type of trichomes, characterized by polar elongation feature. Cotton fibers can be used to cell elongation in polar region, cell wall composition, and ovule fertilization. This helps in improving plant reproduction and production under abiotic stress conditions. Under drought stress, water limitation is a major setback, and development of extra root hairs is plant adaptive mechanism to increase water uptake. Root hairs are also important single-cell type models, used to study mitosis and meiosis and plant resistance to drought and salinity stresses (Kiegle et al., 2000; Comas et al., 2013). Several studies also showed positive role of root hairs in nutrient uptake under nutrient-deficiency stress (Gilroy and Jones, 2000; Jungk, 2001; Ma et al., 2001). Root hairs also help in root anchorage and in development of strong symbiotic relationship as root hairs are the first plant cell types in legumes, which primarily got infected by symbiotic bacteria during nodulation process (Libault et al., 2010). Trichomes can be categorized into two subcategories: glandular and nonglandular trichomes. Glandular trichomes are specialized cell structures that produce or excrete different metabolites, while nonglandular trichomes can store toxic substances and protect plant from stress conditions. Studies revealed that trichomes are very useful models to examine plant responses to abiotic stresses (Lusa et al., 2015; Bergua et al., 2016). Glandular trichomes have been studied to examine the production of secondary metabolites (such as terpenes) and their protective role under abiotic stress conditions (Snyder et al., 1993; Kennedy, 2003). Nonglandular or nonsecretory trichomes such as salt glands are very important models to study salinity stress tolerance and salt accumulation in plants (Harada et al., 2010). Halophytic plants (e.g., quinoa) developed gigantic bladder cells and store salts under salinity stress (Shabala and Mackay, 2011). These bladder cells are

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10 times larger than normal epidermal cell and can store 1000 times more salts (especially Na1) than normal cell vacuoles (Shabala et al., 2014). According to Barkla et al. (2002), increased Na1 accumulation in the vacuole of bladder cells is primarily associated with high V-ATPase activity and tonoplast Na1/H1 antiport. Trichomes are very important models to study salt-stress tolerance mechanisms in halophytes; however, molecular identity and modes of control of key transport systems in salt bladders are not identified yet.

23.3 Computational biology to study plant single-cell responses and abiotic stress tolerance For better understanding of plant single-cell responses under abiotic stresses, it involves the combination of several data sets relating to different cell functions and responses to stress environment (Fig. 23.1B). Development of new approaches and algorithms is a very intense computational effort, and it would help to study complex mechanism in plant responses to abiotic stresses. These new approaches will further understand the response

FIGURE 23.1

Systematic diagram of (A) single-cell genomic analysis and (B) plant single-cell biology

approach.

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of single cell to abiotic stresses. Different models, such as the agricultural production systems simulator, AquaCrop, and decision support system for agrotechnology transfer, have been used so far to study whole plant response to different nutrient supplies (Basak et al., 2010; Liu et al., 2011), water deficit conditions (Chenu et al., 2008; Lopez-Cedron et al., 2008; Liu et al., 2010), or temperature regimes (Asseng et al., 2004; Steduto et al., 2009). Furthermore, several other methods have been developed so far to analyze gene expressions at different levels of organ or tissue. Nonetheless, these traditional methods to analyze transcriptomics at whole plant level are not feasible for single-cell transcriptomic data. Studies would be very useful when using single-cell plant models and study abiotic stress responses. Nonetheless, there are some limitations while studying single-cell responses under abiotic stresses. To date, only 10% of cells have been sequenced in singlecell RNA-sequencing library (Islam et al., 2014), but it is not sufficient when studies deal with low-expressed genes at single-cell level, leading to technical noise. This technical noise can be decreased by examining technical variability using unique molecular identifier, external RNA control consortium, and random nucleotide sequencing (Jiang et al., 2011; Islam et al., 2014). Recent development of algorithm-based techniques such as census made it easy to examine gene expression at single-cell level without using abovementioned techniques (Qiu et al., 2017a). Another limitation of plant single-cell biology is related to difficulties accessing real replicates per se (Kolodziejczyk et al., 2015), and such limitation can be solved by identifying or estimating numerous genes or by examining transcriptomics variability other than technical variability (Bacher and Kendziorski, 2016). Recently, different algorithms (e.g., Waterfall, Sincell, Oscope, Wanderlust, and Monocle) have been designed to study single cells according to their molecular features (Bendall et al., 2014; Trapnell et al., 2014; Shin et al., 2015; Julia et al., 2015; Leng et al., 2015; Qiu et al., 2017b). These approaches help in understanding the complex processes, and this would also lead to understand specific responses of different single cells to same environmental stresses.

23.4 Techniques to study single-cell response to abiotic stress Several limitations have been encountered while studying abiotic stresses in plants at single-cell level; however, developing techniques and technologies make it more convenient to understand the omics single cells than bulk population of cells under stress conditions. Significant research has been done so far in animal and microbial cells (Hu et al., 2016; Neu et al., 2017), but little research has been done in the plant kingdom especially under abiotic stress conditions. Major reason for not doing research at single-cell level in plants was due to the difficulty of isolation of homogenous cells from a heterogeneous cell population and also multiple cell states at different developmental stages under different environments. Several approaches have been designed to isolate and analyze individual cell from bulk cell population. In this section, we have discussed two approaches such as single-cell genetic (SCG) analysis and microelectrode ion flux estimation (MIFE) due to their increasing interest in plant science and abiotic stress tolerance.

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23.4.1 Microelectrode ion flux estimation technique Understanding ionic homeostasis is of extreme importance under abiotic stress conditions. Abiotic stress impairs membrane transport of nutrients across major membranes. In plants, biological membranes exhibit numerous essential cell processes such as cell turgor, nutrient movement and accumulation, ionic homeostasis, cellular signaling, and waste secretion. Changes in the potential or variation plasma membrane in different ion fluxes are among early cellular response to abiotic stresses (Zhu, 2002; Wherrett et al., 2005). In addition, cellular membrane transporters act as ultimate effectors as well as receptormediating plant environment interactions. For instance, under salt stress, exclusion of Na1 from cytosol or compartmentalization in vacuole (Apse et al., 1999; Zhu, 2003) or under Al31 stress variation in malate flux across plasma membrane (Ryan et al., 2001) are examples of potential role of membrane transporters to abiotic stress at single-cell level. Furthermore, such crucial role of membrane transporters in plant cells makes them potential targets for enhancing abiotic stress tolerance in plants. A drawback while studying membrane transporters at single-cell level is associated with complex and heterogeneous network of large number of transporters in plant cells (Shabala, 2006). Recent advances in plant cell biology and plant electrophysiology result in the development of very useful probes that can examine transport of different ions across cell membranes. Noninvasive ion-selective microelectrode probe (MIFE) technique, that is one of them, can successfully help to study differential activities of different ion transporters under different stress conditions (Shabala and Newman, 1997; Shabala et al., 1998; Newman, 2001; Shabala, 2000). MIFE allows the quantification of net ion fluxes across membranes (Shabala et al., 2000; Shabala, 2006). MIFE technique is very useful to study plant single-cell response to abiotic stresses due to five features including (1) MIFE lets in vitro measurement of ion fluxes under physiologically representative conditions, (2) high temporal resolution, (3) high spatial resolution, (4) period of measurement, and (5) concurrent measurement of different ions at specific cell (Shabala, 2006). All these features make MIFE technique a very useful and effective approach to study ionic homeostasis in plant cells and tissues under different abiotic stresses. Theory of MIFE technique has been explained in Newman (2001), and detailed protocol has been provided in Wu et al. (2015). Under stress conditions, there are different ion concentrations in the proximity of cell surface, some ions would be up taken by living cells and some ion would be extruded thus resulting in pronounced electrochemical potential gradient near to cell surface. MIFE can measure such electrochemical potential gradient by moving ion-selective electrode probes between two positions. At each position, electrode voltage is noted and then converted into approximate concentration based on the Nernst equation (Newman, 2001). 23.4.1.1 Usage of microelectrode ion flux estimation to study cell response under abiotic stresses 23.4.1.1.1 Salt stress

Salt stress is one of most detrimental environmental stresses, which causes ionic toxicity, osmotic stress, and oxidative stress simultaneously (Tanveer and Shabala, 2018). Salt tolerance or salt-stress adaptation in glycophytes is associated with the number of

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adaptive mechanisms, and most of them are associated with ion transport. K1 retention and Na1 exclusion are the major key factors involved in salt-stress tolerance (Tanveer and Shah, 2017). MIFE technique helps to understand influx of these major ions across membranes under salt stress, thus providing insights for breeders to develop more salt tolerant plant species. MIFE technique has been used by different researchers to study detrimental effects and salt-stress tolerance mechanism of different abiotic stresses, including salt, waterlogging, and oxidative stresses (Table 23.1). In a study, Shabala and Newman (1997) employed MIFE technique to study K1 flux and to differentiate ionic and osmotic stresses induced by salt stress. Recently, cytosolic K1 retention ability in leaf mesophyll has emerged as an important component of plant salt-tolerance mechanism (Wu et al., 2013). Wu et al. (2015) used MIFE technique as screening tool to screen plants for salt-stress tolerance, and they showed that MIFE is a very useful technique to study salt-stress tolerance at plant cell level. Similarly, Wang et al. (2018) showed that examining the oxidative effects of reactive oxygen species (ROS) on K and Ca fluxes under salt stress could be a useful approach to improve the salt-stress tolerance in barley. 23.4.1.1.2 Water deficit and oxygen deprivation

Water deficit, also termed drought, is often associated with high salt accumulation in upper soil surface, high soil temperature in rhizosphere, and imbalanced nutrient availability (Anjum et al., 2016a, 2017a). It is well known that drought stress significantly reduced photosynthesis and net assimilation, and different reasons have been reported so far (Anjum et al., 2017b). In a study, Mak et al. (2014) used MIFE to study steady-state flux of K1 and Ca21 from leaf mesophyll cells and found large efflux of K1 and Ca21, which serve as chemical signals to induce other drought stress tolerance mechanisms in soybean. Similarly, Feng et al. (2016) used MIFE to study drought stress tolerance among two genotypes of barley and identified drought-tolerant genotype. They found drought-tolerant genotype by examining ionic homeostasis and chemical signals from root cells under drought. Oxygen deprivation due to waterlogging is one of the major abiotic stresses, limiting agricultural productivity worldwide. Plants lose essential nutrients such K1 from cell; however, retaining sufficient K1 in root cells is vital for survival under hypoxia. In a study, MIFE technique was used to study the effects of secondary metabolites on net fluxes of different monovalent and divalent cations from barley root cells under waterlogging stress (Pang et al., 2007). Moreover, Pang et al. (2006) measured variations in net K1 and H1 fluxes under hypoxia using MIFE from root cells. In another study, Zeng et al. (2014) employed MIFE and studied kinetics of K1 flux and membrane potential of root cells under waterlogging stress and found that maintaining significant levels of cytosolic K1 is important for plant survival under waterlogging. 23.4.1.1.3 Aluminum stress

Aluminum toxicity is one of major and most detrimental heavy metal stresses, and trivalent Al ion is most toxic in root rhizosphere (Anjum et al., 2016b,c). Moreover, the extent of Al toxicity reaches to peak effects under low soil pH (pH 4.2 4.3) (Taylor et al., 2000), thus results in Al31 toxicity and soil acidity simultaneously. It was noted that low pH induced significant damages to Arabidopsis roots in a way being

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TABLE 23.1 Role of microelectrode ion flux estimation (MIFE) in studying abiotic stress effects and tolerance mechanisms in plants. Abiotic stress

Role of MIFE in study stress tolerance

References

Salt stress

Showed key role of inorganic ions in plant cell osmoregulation

Chen et al. (2007a,b), Shabala and Cuin (2008)

Salt stress

Revealed specific role of MAPK and SOS1 in stress signaling

Shabala (2006), Lew et al. (2006)

Salt stress

Showed plant’s ability to retain cytosolic K1 as central salt tolerance mechanism

Shabala and Cuin (2008), Chen et al. (2005, 2007a,b)

Salt stress

Showed key role of membrane transporters such as NSCC, GORK, AKT, and SOS1 in adaptation to stress

Shabala and Cuin (2008), Shabala (2006), Chen et al. (2007a,b); Cuin and Shabala (2007)

Salt stress

Examined ameliorative effects of divalent cations on ionic homeostasis under salt stress

Shabala et al. (2003, 2005a,b)

Salt stress

Examined ameliorative effects of compatible solutes on ionic homeostasis under salt stress

Cuin and Shabala (2005, 2007)

Salt stress

Examined ameliorative effect of polyamines on ionic homeostasis under salt stress

Shabala et al. (2007), Pandolfi et al. (2010)

Salt stress

Identified genetic differences of salt-stress tolerance in different crops

Chen et al. (2005, 2008)

Oxidative stress

Showed the role of GORK and NSCC channels in oxidative stress signaling and responses

Demidchik et al. (2002, 2003, 2010)

Oxidative stress by Explored spatial and temporal heterogeneity and H2O2 and OH differential sensitivity of NSCC channels to H2O2 radical and OH radical

Demidchik et al. (2002, 2003, 2007)

Salt stress

Explored the role of GORK and NSCC channels in salt stress-induced programmed cell death

Shabala (2009), Demidchik et al. (2010)

Salt stress

Identified the central role of H1-ATPase in posttranslational regulation in plant cells

Chen et al. (2007a,b)

Waterlogging stress

Revealed the effects of waterlogging on ionic homeostasis

Pang et al. (2006)

Aluminum stress

Identified new temporal and spatial information on the Al31-induced K1 efflux from intact plants

Wherrett et al. (2005)

Drought stress

Identified flux of K1 and Ca21 as chemical signals Mak et al. (2014)

GORK, guard cell outward rectifying potassium channel; MAPK, Mitogen-activated protein kinase; NSCC, nonselective cation channel; OH radical, hydroxyl radical; SOS, salt overly sensitive; AKT, high affinity potassium transporter.

different from damages induced by Al31 stress (Koyama et al., 2001). MIFE technique is very useful in studying Al31 toxicity and soil acidity induced effects on ionic homeostasis and other plant physiological traits. Recently, experiments based on MIFE revealed that low-pH stress induces H1 influx causing alkalinization in rhizosphere, while Al31

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toxicity inhibits H1 influx and reduces alkalinization in rhizosphere. Moreover, Al31 toxicity results in the release of different organic anions particularly K1 (Ryan et al., 2001); however, it was not yet identified as the most sensitive root zone. In a study, MIFE technique identified that elongation zone as most sensitive zone in root, providing new temporal and spatial information on the Al31, induced K1 efflux from intact plants (Wherrett et al., 2005).

23.4.2 Single-cell genomic analysis In living organism, individual living cells exhibit highly variable cellular response and processes. Advances in nucleotide-sequencing technologies helped to perform genomic analysis and functional characterization of individual cells under different environmental stimuli. SCG analysis has been widely employed to study genomics in mammalian cells; however, application of SCG is on its early stages. There is a great prospective to investigate individual cell responses especially pre- and posttranslational and transcriptional alterations in individual cells under stress conditions. SCG analysis, when combined with RNA sequencing, provides more insights into gene expression levels at single-cell levels (Yuan et al., 2018). Such sequencing technologies help in high-resolution measurement of intercell variation that otherwise is hidden in conventional bulk sequencing. SCG analysis comprises four basic steps (Fig. 23.1A): (1) single-cell suspension and isolation from plant tissues, (2) extraction of DNA and RNA, (3) DNA amplification and DNA sequencing, and (4) bioinformatics analysis. Different techniques have been employed at each step, and Yuan et al. (2018) reviewed and documented significant information relating SCG analysis in plant science. Briefly, techniques, such as fluorescenceactivated cell sorting, laser microdissection, laser capture microdissection, microfluidics, serial dilution, and magnetic-activated cell sorting, are used for single-cell suspension and isolation (Emmert-Buck et al., 1996; Whitesides, 2006; Dean et al., 2002; Shapiro et al., 2013). All these approaches work differentially using different enzymes and digestion proteins, and every approach has its own advantage and limitation. For instance, high costs for magnetic separation in magnetic-activated cell sorting, the columns and antibodies used in sorting, and the specific sensitivity cell populations make its usage far more limited than fluorescence-activated cell sorting (Hu et al., 2016). The extraction of DNA and RNA can be carried using different commercially available DNA- and RNA-extraction kits. DNA amplification and sequencing can be carried out by multiple displacement amplification, microwell displacement amplification system, and polymerase chain reaction (PCR) (Dean et al., 2002; Gole et al., 2013). For bioinformatics analysis, single-cell DNA and RNA are sequenced for genomic analysis. In animals, these sequencing approaches have been used extensively; however, in plants, only two studies have been conducted so far on Arabidopsis root cells and classify cells using clustering (Brennecke et al., 2013; Efroni et al., 2015). Plant cells are very specific and exhibit very specialized morphophysiological features (Nelson et al., 2008). In Arabidopsis, high-resolution gene expression analysis showed that gene expression patterns in Arabidopsis root cells do not always correlate with previously identified individual cell anatomical features (Birnbaum et al., 2003; Brady et al., 2007).

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Similar results have been reported in leaf epidermis cells of maize (Nakazono et al., 2003) and barley (Lu et al., 2002). SCG analysis has also explained the development and differentiation of plant morphological traits for example, stomatal cells (Adrian et al., 2015), pollen (Becker et al., 2003; Honys and Twell, 2003), and female gametophytes (Schmid et al., 2015). Gene expression analysis of plant single cell under different stress conditions suggested tight gene regulation. For instance, transcript levels of Arabidopsis root cells were specific to different developmental stages under salt stress (Dinneny et al., 2008). In another study, differential nitrogen influx pattern was observed in five Arabidopsis root cells (Gifford et al., 2008). Plant single-cell models (e.g., trichomes, pollen, cotton fibers, or bladder cells) are easy to handle and analyze using single-cell technology as compared in animals. These plant single-cell models facilitate high-resolution gene analysis and increase our understanding regarding cell responses under different abiotic stress conditions. Plant cells exhibit significant variations during development (Day et al., 2002); however, it is unclear whether plant cell-fate regulation is a lineage-dependent mechanism or based on cell relative position (Kidner et al., 2000). SCG analysis can also be employed to examine specific cell stage during different cell developmental stages, thus revealing regeneration mechanisms and cell fate under abiotic stresses. Recently, single-cell analysis has shown that different Arabidopsis cells rapidly redevelop stem cell via reprogramming embryogenesis (Efroni et al., 2016), therefore highlighting the role of central cell growth system in plants (Rahni et al., 2016). SCG analysis can also help in identifying key genes in cell regeneration, which can be further used as marker for crop breeding. In conclusion, SCG analysis can help in the identification of novel genes and transcripts in plant single cells, which would be very useful for improving stress tolerance and for modeling generegulatory networks.

23.5 Concluding remarks Plant single-cell biology is very useful and provides a new opportunity to investigate plant single-cell responses under different abiotic stresses. Development of new technologies and computer algorithms makes it more convenient to study plant single-cell biology and understand different physiological and genetic processes in individual cells. In animals, single-cell analysis has been conducted from long time; however, it was difficult to isolate and study plant single cell due to their heterogeneity. Recent studies employed cotton fibers, trichomes, root hairs, guard cells, and pollens as single cells and identified numerous plant physiological processes such as ionic homeostasis at plant cell membrane level to study abiotic stress effects and responses in plant single cells. One setback during studying plant single-cell and abiotic responses is their heterogeneous nature, and it is difficult to isolate and analyze individual plant cells. However, recent development in plant electrophysiology and plant transcriptomics reduced this difficulty to a significant level. Two approaches, such as SCG analysis and MIFE, provide new insights in understanding plant single-cell responses and abiotic stress tolerance mechanisms in plants. Future research should be focused on using these approaches and understanding stress signaling and signal propagation in plant single cell.

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References

621

References Adrian, J., Chang, J., Ballenger, C.E., Bargmann, B.O., Alassimone, J., Davies, K.A., et al., 2015. Transcriptome dynamics of the stomatal lineage: birth, amplification, and termination of a self-renewing population. Dev. Cell. 33, 107 118. Alberts, B., Bray, D., Hopkin, K., Johnson, A., Lewis, J., Raff, M., et al., 2013. Essential Cell Biology. Garland Science. Amme, S., Rutten, T., Melzer, M., Sonsmann, G., Vissers, J.P.C., Schlesier, B., et al., 2005. A proteome approach defines protective functions of tobacco leaf trichomes. Proteomics 5, 2508 2518. Anjum, S.A., Tanveer, M., et al., 2016a. Effect of progressive drought stress on growth, leaf gas exchange, and antioxidant production in two maize cultivars. Environ. Sci. Pollut. Res. 23 (17), 17132 17141. Anjum, S.A., Ashraf, U., Khan, I., Tanveer, M., et al., 2016b. Aluminum and chromium toxicity in maize: implications for agronomic attributes, net photosynthesis, physio-biochemical oscillations, and metal accumulation in different plant parts. Water Air Soil Pollut. 227 (9), 326. Anjum, S.A., Ashraf, U., Khan, I., Tanveer, M., et al., 2016c. Chromium and aluminum phytotoxicity in maize: morpho-physiological responses and metal uptake. CLEAN Soil Air Water 44 (8), 1075 1084. Anjum, S.A., Ashraf, U., Zohaib, A., Tanveer, M., Naeem, M., Iftikhar, A.L.I., et al., 2017a. Growth and developmental responses of crop plants under drought stress: a review. Zemdirbyste-Agric. 104, 267 276. Anjum, S.A., Ashraf, U., Tanveer, M., Khan, I., Hussain, S., Shahzad, B., et al., 2017b. Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front. Plant Sci. 8, 69. Available from: https://doi.org/10.3389/fpls.2017.00069. Apse, M.P., Aharon, G.S., Snedden, W.A., Blumwald, E., 1999. Salt tolerance conferred by overexpression of a vacuolar Na1/H1 antiport in Arabidopsis. Science 285, 1256 1258. Arpat, A.B., et al., 2004. Functional genomics of cell elongation in developing cotton fibers. Plant Mol. Biol. 54, 911 929. Asseng, S., Jamieson, P.D., Kimball, B., Pinter, P., Sayre, K., Bowden, J.W., et al., 2004. Simulated wheat growth affected by rising temperature, increased water deficit and elevated atmospheric CO2. Field Crops Res. 85 (2 3), 85 102. Aziz, N., Paiva, N.L., May, G.D., Dixon, R.A., 2005. Transcriptome analysis of alfalfa glandular trichomes. Planta 221, 28 38. Bacher, R., Kendziorski, C., 2016. Design and computational analysis of single-cell RNA-sequencing experiments. Genome Biol. 17, 63. Barkla, B.J., Vera-Estrella, R., Camacho-Emiterio, J., Pantoja, O., 2002. Na1/H1 exchange in the halophyte Mesembryanthemum crystallinum is associated with cellular sites of Na1 storage. Funct. Plant Biol. 29, 1017 1024. Basak, J.K., Ali, M.A., Islam, M.N., Rashid, M.A., 2010. Assessment of the effect of climate change on boro rice production in Bangladesh using DSSAT model. J. Civ. Eng. 38, 95 108. Becker, J.D., Boavida, L.C., Carneiro, J., Haury, M., Feijo, J.A., 2003. Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol. 133, 713 725. Bendall, S.C., et al., 2014. Single-cell trajectory detection uncovers progression and regulatory coordination in human B cell development. Cell 157, 714 725. Bergau, N., et al., 2016. Autofluorescence as a signal to sort developing glandular trichomes by flow cytometry. Front. Plant Sci. 7, 949. Bertea, C.M., Voster, A., Verstappen, F.W.A., Maffei, M., Beekwilder, J., Bouwmeester, H.J., 2006. Isoprenoid biosynthesis in Artemisia annua: cloning and heterologous expression of a germacrene A synthase from a glandular trichome cDNA library. Arch. Biochem. Biophys. 448, 3 12. Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung, J.W., Lambert, G.M., Galbraith, D.W., et al., 2003. A gene expression map of the Arabidopsis root. Science 302, 1956 1960. Brady, S.M., Orlando, D.A., Lee, J.Y., Wang, J.Y., Koch, J., Dinneny, J.R., et al., 2007. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318, 801 806. Brennecke, P., Anders, S., Kim, J.K., Kolodziejczyk, A.A., Zhang, X., Proserpio, V., et al., 2013. Accounting for technical noise in single-cell RNA-seq experiments. Nat. Methods 10, 1093 1095. Chaves, M.M., Maroco, J.P., Pereira, J.S., 2003. Understanding plant responses to drought—from genes to the whole plant. Funct. Plant Biol. 30 (3), 239 264.

Plant Life under Changing Environment

622

23. Plant single-cell biology and abiotic stress tolerance

Chen, Z., Newman, I., Zhou, M., Mendham, N., Zhang, G., Shabala, S., 2005. Screening plants for salt tolerance by measuring K1 flux: a case study for barley. Plant Cell Environ. 28, 1230 1246. Chen, Z.H., Shabala, S., Mendham, N., Newman, I., Zhang, G.P., Zhou, M.X., 2008. Combining ability of salinity tolerance on the basis of NaCl induced K1 flux from roots of barley. Crop Sci. 48, 1382 1388. Chen, Z.H., Cuin, T.A., Zhou, M., Twomey, A., Naidu, B., Shabala, S., 2007a. Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J. Exp. Bot. 58, 4245 4255. Chen, Z.H., Pottosin, I.I., Cuin, T.A., Fuglsang, A.T., Tester, M., Jha, D., et al., 2007b. Root plasma membrane transporters controlling K1/Na1 homeostasis in salt-stressed barley. Plant Physiol. 145, 1714 1725. Chenu, K., Chapman, S.C., Hammer, G.L., Mclean, G., Salah, H.B.H., Tardieu, F., 2008. Short-term responses of leaf growth rate to water deficit scale up to whole-plant and crop levels: an integrated modelling approach in maize. Plant Cell Environ. 31 (3), 378 391. Comas, L., Becker, S., Cruz, V.M.V., Byrne, P.F., Dierig, D.A., 2013. Root traits contributing to plant productivity under drought. Front. Plant Sci. 4, 442. Cuin, T.A., Shabala, S., 2005. Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol. 46, 1924 1933. Cuin, T.A., Shabala, S., 2007. Amino acids regulate salinity-induced potassium efflux in barley root epidermis. Planta 225, 753 761. Day, M.E., Greenwood, M.S., Diaz-Sala, C., 2002. Age-and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. Tree Physiol. 22 (8), 507 513. Dean, F.B., Hosono, S., Fang, L., Wu, X., Faruqi, A.F., Bray-Ward, P., et al., 2002. Comprehensive human genome amplification using multiple displacement amplification. Proc. Natl. Acad. Sci. U.S.A. 99, 5261 5266. Demidchik, V., Bowen, H.C., Maathuis, F.J.M., Shabala, S.N., Tester, M.A., White, P.J., et al., 2002. Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. Plant J. 32, 799 808. Demidchik, V., Shabala, S.N., Coutts, K.B., Tester, M.A., Davies, J.M., 2003. Free oxygen radicals regulate plasma membrane Ca21 and K1-permeable channels in plant root cells. J. Cell Sci. 116, 81 88. Demidchik, V., Shabala, S.N., Davies, J.M., 2007. Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca21 flux and plasma membrane Ca21 channels. Plant J. 49, 377 386. Demidchik, V., Cuin, T.A., Svistunenko, D., Smith, S.J., Miller, A.J., Shabala, S., et al., 2010. Arabidopsis root K1efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J. Cell Sci. 123, 1468 1479. Dinneny, J.R., Long, T.A., Wang, J.Y., Jung, J.W., Mace, D., Pointer, S., et al., 2008. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320, 942 945. Efroni, I., Ip, P.L., Nawy, T., Mello, A., Birnbaum, K.D., 2015. Quantification of cell identity from single-cell gene expression profiles. Genome. Biol. 16, 9. Efroni, I., Mello, A., Nawy, T., Ip, P.L., Rahni, R., DelRose, N., et al., 2016. Root regeneration triggers an embryolike sequence guided by hormonal interactions. Cell 165, 1721 1733. Emmert-Buck, M.R., Bonner, R.F., Smith, P.D., Chuaqui, R.F., Zhuang, Z., Goldstein, S.R., et al., 1996. Laser capture microdissection. Science 274, 998 1001. Feng, X., Liu, W., Zeng, F., Chen, Z., Zhang, G., Wu, F., 2016. K1 Uptake, H1-ATPase pumping activity and Ca21 efflux mechanism are involved in drought tolerance of barley. Environ. Exp. Bot. 129, 57 66. Garcia-Mata, C., Gay, R., Sokolovski, S., Hills, A., Lamattina, L., Blatt, M.R., 2003. Nitric oxide regulates K1 and Cl-channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 100 (19), 11116 11121. Gawad, C., et al., 2016. Single-cell genome sequencing: current state of the science. Nat. Rev. Genet. 17, 175 188. Geiger, D., Scherzer, S., Mumm, P., Stange, A., Marten, I., Bauer, H., et al., 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc. Natl. Acad. Sci. U.S.A. 106 (50), 21425 21430. Gifford, M.L., Dean, A., Gutierrez, R.A., Coruzzi, G.M., Birnbaum, K.D., 2008. Cell-specific nitrogen responses mediate developmental plasticity. Proc. Natl. Acad. Sci. U.S.A. 105, 803 808. Gilroy, S., Jones, D.L., 2000. Through form to function: root hair development and nutrient uptake. Trends Plant Sci. 5 (2), 56 60. Gole, J., Gore, A., Richards, A., Chiu, Y.J., Fung, H.L., Bushman, D., et al., 2013. Massively parallel polymerase cloning and genome sequencing of single cells using nanoliter microwells. Nat. Biotechnol. 31, 1126 1132.

Plant Life under Changing Environment

References

623

Gutierre´z-Alcala´, G., Gotor, C., Meyer, A.J., Fricker, M., Vega, J.M., Romero, L.C., 2000. Glutathione biosynthesis in Arabidopsis trichome cells. Proc. Natl. Acad. Sci. U.S.A. 97, 11108 11113. Hamamura, Y., et al., 2011. Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana. Curr. Biol. 21, 497 502. Harada, E., Kim, J.A., Meyer, A.J., Hell, R., Clemens, S., Choi, Y.E., 2010. Expression profiling of tobacco leaf trichomes identifies genes for biotic and abiotic stresses. Plant Cell Physiol. 51 (10), 1627 1637. Honys, D., Twell, D., 2003. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 132, 640 652. Hu, P., Zhang, W., Xin, H., Deng, G., 2016. Single cell isolation and analysis. Front. Cell Dev. Biol. 4, 116. Hussain, M., Farooq, S., Hasan, W., Ul-Allah, S., Tanveer, M., Farooq, M., et al., 2018a. Drought stress in sunflower: physiological effects and its management through breeding and agronomic alternatives. Agric. Water Manage. 201, 152 166. Hussain, S., Khaliq, A., Tanveer, M., Matloob, A., Hussain, H.A., 2018b. Aspirin priming circumvents the salinityinduced effects on wheat emergence and seedling growth by regulating starch metabolism and antioxidant enzyme activities. Acta Physiol. Plant. 40 (4), 68. Irving, H.R., Gehring, C.A., Parish, R.W., 1992. Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc. Natl. Acad. Sci. U.S.A. 89 (5), 1790 1794. Islam, S., et al., 2014. Quantitative single-cell RNA-seq with unique molecular identifiers. Nat. Methods 11, 163 166. Jiang, L., et al., 2011. Synthetic spike-in standards for RNA-seq experiments. Genome Res. 21, 1543 1551. Jin, X.F., et al., 2013. Abscisic acid-responsive guard cell metabolomes of arabidopsis wild-type and gpa1 G-protein mutants. Plant Cell 25, 4789 4811. Julia´, M., et al., 2015. Sincell: an R/Bioconductor package for statistical assessment of cell-state hierarchies from single-cell RNA-seq. Bioinformatics 31, 3380 3382. Jungk, A., 2001. Root hairs and the acquisition of plant nutrients from soil. J. Plant Nutr. Soil Sci. 164 (2), 121 129. Kennedy, G.G., 2003. Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu. Rev. Entomol. 48, 51 72. Kidner, C., Sundaresan, V., Roberts, K., Dolan, L., 2000. Clonal analysis of the Arabidopsis root confirms that position, not lineage, determines cell fate. Planta 211, 191 199. Kiegle, E., Moore, C.A., Haseloff, J., Tester, M.A., Knight, M.R., 2000. Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J. 23 (2), 267 278. Kolodziejczyk, A.A., et al., 2015. The technology and biology of single-cell RNA sequencing. Mol. Cell 58, 610 620. Koyama, H., Toda, T., Hara, T., 2001. Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin-Ca interaction may play an important role in proton rhizotoxicity. J. Exp. Bot. 52, 361 368. Kroumova, A.B., Shepherd, R.W., Wagner, G.J., 2007. Impacts of phylloplanin gene knockdown and of Helianthus and Datura phylloplanins on Peronospora tabacina spore germination and disease potential. Plant Physiol. 144, 1843 1851. Leng, N., et al., 2015. Oscope identifies oscillatory genes in unsynchronized single-cell RNA-seq experiments. Nat. Methods 12, 947 950. Lew, R.R., Levina, N.N., Shabala, L., Anderca, M.I., Shabala, S.N., 2006. Role of a mitogen-activated protein kinase cascade in ion flux-mediated turgor regulation in fungi. Eukaryot. Cell 5, 480 487. Libault, M., et al., 2010. Root hair systems biology. Trends Plant Sci. 15, 641 650. Libault, M., Pingault, L., Zogli, P., Schiefelbein, J., 2017. Plant systems biology at the single-cell level. Trends Plant Sci. 22 (11), 949 960. Liu, H.L., Yang, J.Y., Tan, C.S., Drury, C.F., Reynolds, W.D., Zhang, T.Q., et al., 2011. Simulating water content, crop yield and nitrate-N loss under free and controlled tile drainage with subsurface irrigation using the DSSAT model. Agric. Water Manage. 98 (6), 1105 1111. Lopez-Cedron, F.X., Boote, K.J., Pin˜eiro, J., Sau, F., 2008. Improving the CERES-Maize model ability to simulate water deficit impact on maize production and yield components. Agron. J. 100 (2), 296 307. Lu, C., Koroleva, O.A., Farrar, J.F., Gallagher, J., Pollock, C.J., Tomos, A.D., 2002. Rubisco small subunit, chlorophyll a/b-binding protein and sucrose:fructan-6-fructosyl transferase gene expression and sugar status in single barley leaf cells in situ. Cell type specificity and induction by light. Plant Physiol. 130, 1335 1348. Luan, S., 2002. Signalling drought in guard cells. Plant Cell Environ. 25 (2), 229 237.

Plant Life under Changing Environment

624

23. Plant single-cell biology and abiotic stress tolerance

Lusa, M.G., et al., 2015. Trichomes related to an unusual method of water retention and protection of the stem apex in an arid zone perennial species. AoB Plants 7, plu088. Ma, Z., Bielenberg, D.G., Brown, K.M., Lynch, J.P., 2001. Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ. 24 (4), 459 467. Mak, M., Babla, M., Xu, S.C., O’Carrigan, A., Liu, X.H., Gong, Y.M., et al., 2014. Leaf mesophyll K1, H1 and Ca21 fluxes are involved in drought-induced decrease in photosynthesis and stomatal closure in soybean. Environ. Exp. Bot. 98, 1 12. Marks, M.D., et al., 2008. A new method for isolating large quantities of Arabidopsis trichomes for transcriptome, cell wall and other types of analyses. Plant J. 56, 483 492. McCormick, S., 2013. Pollen. Curr. Biol. 23, R988 R990. Nagel, J., Culley, L.K., Lu, Y., Liu, E., Matthews, P.D., Stevens, J.F., et al., 2008. EST analysis of hop glandular trichomes identifies an O-methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell 20, 186 200. Nakazono, M., Qiu, F., Borsuk, L.A., Schnable, P.S., 2003. Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15, 583 596. Nelson, T., Gandotra, N., Tausta, S.L., 2008. Plant cell types: reporting and sampling with new technologies. Curr. Opin. Plant Biol. 11, 567 573. Neu, K.E., et al., 2017. Single-cell genomics: approaches and utility in immunology. Trends Immunol. 38, 140 149. Newman, I.A., 2001. Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant Cell Environ. 24, 1 14. Pandolfi, C., Pottosin, I., Cuin, T., Mancuso, S., Shabala, S., 2010. Specificity of polyamine effects on NaCl-induced ion flux kinetics and salt stress amelioration in plants. Plant Cell Physiol. 51, 422 434. Pang, J.Y., Newman, I., Mendham, N., Zhou, M., Shabala, S., 2006. Microelectrode ion and O 2 fluxes measurements reveal differential sensitivity of barley root tissues to hypoxia. Plant Cell Environ. 29, 1107 1121. Pang, J., Cuin, T., Shabala, L., Zhou, M., Mendham, N., Shabala, S., 2007. Effect of secondary metabolites associated with anaerobic soil conditions on ion fluxes and electrophysiology in barley roots. Plant Physiol. 145 (1), 266 276. Qiao, Z., Libault, M., 2013. Unleashing the potential of the root hair cell as a single plant cell type model in root systems biology. Front. Plant Sci. 4, 484. Qiu, X., et al., 2017a. Single-cell mRNA quantification and differential analysis with Census. Nat. Methods 14, 309 315. Qiu, X., et al., 2017b. Reversed Graph Embedding Resolves Complex Single-Cell Developmental Trajectories. bioRxiv Published online February 21, 2017. Available from: https://doi.org/10.1101/110668. Rahni, R., Efroni, I., Birnbaum, K.D., 2016. A case for distributed control of local stem cell behavior in plants. Dev. Cell. 38, 635 642. Russell, S.D., 1992. Double fertilization. Int. Rev. Cytol. 140, 357 388. Rutley, N., Twell, D., 2015. A decade of pollen transcriptomics. Plant Reprod. 28, 73 89. Ryan, P.R., Delhaize, E., Jones, D.L., 2001. Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 52, 527 560. Schellmann, S., Hu¨lskamp, M., 2005. Epidermal differentiation: trichomes in Arabidopsis as a model system. Int. J. Dev. Biol. 49, 579 584. Schmid, M.W., Schmidt, A., Grossniklaus, U., 2015. The female gametophyte: an emerging model for cell typespecific systems biology in plant development. Front. Plant Sci. 6, 907. Shabala, S., 2000. Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll. Plant Cell Environ. 23, 825 837. Shabala, S., 2006. Non-invasive microelectrode ion flux measurements in plant stress physiology. Plant Electrophysiology. Springer, Berlin, Heidelberg, pp. 35 71. Shabala, S., 2009. Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J. Exp. Bot. 60, 709 711. Shabala, S., Cuin, T.A., 2008. Potassium transport and plant salt tolerance. Physiol. Plant. 133, 651 669.

Plant Life under Changing Environment

References

625

Shabala, S., Mackay, A., 2011. Ion transport in halophytes. Adv. Bot. Res. 57, 151 199. Shabala, S., Newman, I.A., 1997. H1 flux kinetics around plant roots after short-term exposure to low temperature—identifying critical temperatures for plant chilling tolerance. Plant Cell Environ. 20, 1401 1410. Shabala, S., Newman, I., Whittington, J., Juswono, U., 1998. Protoplast ion fluxes: their measurement and variation with time, position and osmoticum. Planta 204, 146 152. Shabala, S., Babourina, O., Newman, I., 2000. Ion-specific mechanisms of osmoregulation in bean mesophyll cells. J. Exp. Bot. 51, 1243 1253. Shabala, S., Shabala, L., Van Volkenburgh, E., 2003. Effect of calcium on root development and root ion fluxes in salinized barley seedlings. Funct. Plant Biol. 30, 507 514. Shabala, S., Shabala, L., Van Volkenburgh, E., Newman, I., 2005a. Effect of divalent cations on ion fluxes and leaf photochemistry in salinized barley leaves. J. Exp. Bot. 56, 1369 1378. Shabala, L., Cuin, T.A., Newman, I.A., Shabala, S., 2005b. Salinity-induced ion flux patterns from the excised roots of Arabidopsis SOS mutants. Planta 222, 1041 1050. Shabala, S., Cuin, T.A., Pottosin, I., 2007. Polyamines prevent NaCl-induced K1 efflux from pea mesophyll by blocking nonselective cation channels. FEBS Lett. 581, 1993 1999. Shabala, S., Bose, J., Hedrich, R., 2014. Salt bladders: do they matter? Trends Plant Sci. 19 (11), 687 691. Shapiro, E., Biezuner, T., Linnarsson, S., 2013. Single-cell sequencing-based technologies will revolutionize wholeorganism science. Nat. Rev. Genet. 14, 618 630. Shepherd, R.W., Bass, W.T., Houtz, R.L., Wagner, G.J., 2005. Phylloplanins of tobacco are defensive proteins deployed on aerial surfaces by short glandular trichomes. Plant Cell 17 1851 1861. Shin, J., et al., 2015. Single-cell RNA-Seq with waterfall reveals molecular cascades underlying adult neurogenesis. Cell Stem Cell 17, 360 372. Simpson, E.H., 1951. The interpretation of interaction in contingency tables. J. R. Stat. Soc. Ser. B: Stat. Methodol. 13, 238 241. Snyder, J.C., et al., 1993. 2,3-Dihydrofarnesoic acid, a unique terpene from trichomes of Lycopersicon hirsutum, repels spider mites. J. Chem. Ecol. 19, 2981 2997. Steduto, P., Hsiao, T.C., Raes, D., Fereres, E., 2009. AquaCrop—the FAO crop model to simulate yield response to water: I. Concepts and underlying principles. Agron. J. 101 (3), 426 437. Tanveer, M., Shabala, S., 2018. Targeting redox regulatory mechanisms for salinity stress tolerance in crops, Salinity Responses and Tolerance in Plants, vol. 1. Springer, Cham, pp. 213 234. Tanveer, M., Shah, A.N., 2017. An insight into salt stress tolerance mechanisms of Chenopodium album. Environ. Sci. Pollut. Res. 24, 16531 16535. Tanveer, M., Shahzad, B., Sharma, A., Biju, S., Bhardwaj, R., 2018. 24-Epibrassinolide; an active brassinolide and its role in salt stress tolerance in plants: a review. Plant. Physiol. Biochem. Available from: https://doi.org/ 10.1016/j.plaphy.2018.06.035. Taylor, G.J., et al., 2000. Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol. 123, 987 996. Trapnell, C., et al., 2014. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381 386. Wagner, G.J., 1991. Secreting glandular trichomes: more than just hairs. Plant Physiol. 96, 675 679. Wagner, G.J., Wang, E., Shepherd, R.W., 2004. New approaches for studying and exploiting and old protuberance, the plant trichome. Ann. Bot. 93, 3 11. Wang, F., Chen, Z.H., Liu, X., Colmer, T.D., Shabala, L., Salih, A., et al., 2016a. Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis. J. Exp. Bot. 68 (12), 3191 3204. Wang, M., et al., 2016b. Multi-omics maps of cotton fibre reveal epigenetic basis for staged single-cell differentiation. Nucleic Acids Res. 44, 4067 4079. Wang, H., Shabala, L., Zhou, M., Shabala, S., 2018. Hydrogen peroxide-induced root Ca21 and K1 fluxes correlate with salt tolerance in cereals: towards the cell-based phenotyping. Int. J. Mol. Sci. 19, 702. Available from: https://doi.org/10.3390/ijms19030702. Wherrett, T., Ryan, P.R., Delhaize, E., Shabala, S., 2005. Effect of aluminium on membrane potential and ion fluxes at the apices of wheat roots. Funct. Plant Biol. 32, 199 208. Whitesides, G.M., 2006. The origins and the future of microfluidics. Nature 442, 368 373.

Plant Life under Changing Environment

626

23. Plant single-cell biology and abiotic stress tolerance

Wienkoop, S., Zoeller, D., Ebert, B., Simon-Rosin, U., Fisahn, J., Glinski, M., et al., 2004. Cell-specific protein profiling in Arabidopsis thaliana trichomes: identification of trichome-located proteins involved in sulfur metabolism and detoxification. Phytochemistry 65, 1641 1649. Wu, H., Shabala, L., Barry, K., Zhou, M., Shabala, S., 2013. Ability of leaf mesophyll to retain potassium correlates with salinity tolerance in wheat and barley. Physiol. Plant. 149, 515 527. Wu, H., Shabala, L., Zhou, M., Shabala, S., 2015. MIFE technique-based screening for mesophyll K1 retention for crop breeding for salinity tolerance. Bio-protocol 5 (9), 1 10. Wuest, S.E., et al., 2010. Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr. Biol. 20, 506 512. Yang, C.X., Ye, Z.B., 2013. Trichomes as models for studying plant cell differentiation. Cell Mol. Life Sci. 70, 1937 1948. Yuan, Y., Lee, H., Hu, H., Scheben, A., Edwards, D., 2018. Single-cell genomic analysis in plants. Genes 9, 50. Available from: https://doi.org/10.3390/genes9010050. Yule, G.U., 1902. Notes on the theory of association of attributes in statistics. Biometrika 2, 121 134. Zeng, F., Konnerup, D., Shabala, L., Zhou, M., Colmer, T.D., Zhang, G., et al., 2014. Linking oxygen availability with membrane potential maintenance and K1 retention of barley roots: implications for waterlogging stress tolerance. Plant Cell Environ. 37 (10), 2325 2338. Zhu, J.K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant. Biol. 53, 247 273. Zhu, J.K., 2003. Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 6, 441 445.

Further reading Balcerowicz, D., et al., 2015. Cell fate determination and the switch from diffuse growth to planar polarity in Arabidopsis root epidermal cells. Front. Plant Sci. 6, 1163. Elzenga, J.T.M., Keller, C.P., Van Volkenburgh, E., 1991. Patch clamping protoplasts from vascular plants: method for the quick isolation of protoplasts having a high success rate of gigaseal formation. Plant Physiol. 97 (4), 1573 1575. Navin, N., Kendall, J., Troge, J., Andrews, P., Rodgers, L., McIndoo, J., et al., 2011. Tumour evolution inferred by single-cell sequencing. Nature 472, 90 94. Rogers, E.D., Jackson, T., Moussaieff, A., Aharoni, A., Benfey, P.N., 2012. Cell type-specific transcriptional profiling: implications for metabolite profiling. Plant J. 70 (1), 5 17. Schiefelbein, J., et al., 2014. Regulation of epidermal cell fate in Arabidopsis roots: the importance of multiple feedback loops. Front. Plant Sci. 5, 47. Schroeder, J.I., Kwak, J.M., Allen, G.J., 2001. Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410 (6826), 327.

Plant Life under Changing Environment

C H A P T E R

24 Nanoparticle application and abiotic-stress tolerance in plants Mohsin Tanveer1, Babar Shahzad1 and Umair Ashraf2 1

School of Land and Food, University of Tasmania, Hobart, Australia 2Department of Botany, University of Education (Lahore), Faisalabad-Campus, Faisalabad, Pakistan

24.1 Introduction Global warming, anthropogenic activities, and other inevitable factors have caused climate change, resulting in occurrence of numerous abiotic stresses. These abiotic stresses not only reduce agriculture productivity but also result in degradation of natural resources (Shahzad et al., 2016, 2018). Different studies documented significant yield reduction in numerous crops under abiotic-stress conditions (Anjum et al., 2017c; Hussain et al., 2018; Khan et al., 2018). Development and progress in plant science have revealed different aspects and mechanisms of abiotic stresses induced detrimental effects on crop plants. Nonetheless, development in plant physiology and genetics and other applied biological studies developed stress tolerant plants and further showed how plants can be made tolerant to different abiotic stress conditions and what aspects should be further investigated. Nanotechnology is a new and emerging technology, which relies on the application of nanoparticles (NPs) with small radius in order to enhance abiotic-stress tolerance in plants (Moisala et al., 2003). In this chapter, we explained the role and scope of nanotechnology in improving abiotic-stress tolerance in plants. Furthermore, NPs toxicity has also been discussed.

24.2 Uptake, transportation, and translocation of nanoparticles Anthropogenic activities are the sole reason of NPs in soil and can become a main source of NPs for the uptake of terrestrial plants. Plants are considered as a vital and primary element of all the ecosystems and play crucial role in determining the transport and fate of NPs in the environment (Monica and Cremonini, 2009). Metallic NPs such as Cu

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24. Nanoparticle application and abiotic-stress tolerance in plants

oxide NPs have similarity to Cu ionic forms; therefore complex molecules are dissociated from their complex form into simpler forms to become readily available to plants (Adrees et al., 2015). In roots, subrenization of exodermis and endodermis hindrances NPs uptake; nevertheless, development of lateral roots enables the apoplastic bypass further facilitating the entry of NPs into the xylem (Dietz and Herth, 2011; Shaw and Hossain, 2013). Moreover, transportation of NPs takes place from the root to the shoot via xylem and from shoot to the root via phloem. Metal accumulation takes place in apoplastic region because it is the major section for metal accumulation (Krzesłowska, 2011). Nekrasova et al. (2011) tested that plants more actively accumulate Cu ions than CuO-NPs due to small radius and higher penetration capacity of Cu. Accumulation of NPs in the root and shoot system induces the formation of different reactive oxygen species (ROS) (Dietz and Herth, 2011; Shaw and Hossain, 2013).

24.2.1 Nanoparticle application and oxidative stress tolerance Under abiotic conditions, limitation of oxygen supply and excitation of electrons cause high production of active oxygen species (Demidchik, 2015). These ROS can damage biological membranes and disrupt numerous physiological processes in plants (Tanveer and Shabala, 2018). Under abiotic-stress conditions, limitation of CO2 assimilation decreases nicotinamide adenine dinucleotide phosphate (NADP1) regeneration, concomitantly, electron transport chain (ETC) gets overreduced, and produces superoxide and singlet oxygen radicals in the chloroplasts (Shao et al., 2008). These ROS not only disrupts biological membranes but also reduced photosynthesis by degrading chlorophyll contents and chloroplast ultrastructures. Therefore due to the highly toxic nature of ROS, their assimilation in plant tissues and/or plant cells must be tightly controlled. Plants exhibit antioxidants defense system that can scavenge ROS and maintain a redox potential in cells (Anjum et al., 2017a,b). Antioxidants, also termed oxidants scavenging enzymes, are very important defense mechanisms in plants, and plants exhibited higher antioxidant activity and showed higher tolerance to abiotic stresses (Tanveer and Shabala, 2018). This section highlighted the role of NPs in redox regulation, their protective role for photosynthesis, and ionic homeostasis under abiotic-stress conditions.

24.3 Nanoparticle application and its role in redox regulation Application of NPs has showed promising results in improving abiotic-stress tolerance in plants via playing crucial role in numerous plant physiological processes such as redox regulation (Table 24.1). For instance, application of nano-silicon improved salt stress tolerance in cherry tomato via activating antioxidant defense system (Haghighi and Pessarakli 2013). Furthermore, under chromium stress, silicon NPs (Si-NPs) protected pea plants from oxidative damage via enhancing production of antioxidants such as super dimutase (SOD), peroxidase (POD), and catalase (CAT) (Tripathi et al., 2015). Si-NPs have been reported as protecting agents that can protect chlorophyll and carotenoids from heavy metal induced oxidative damage (Tripathi et al., 2015). In another study, it has been

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24.3 Nanoparticle application and its role in redox regulation

TABLE 24.1

Positive effects of nanoparticles application on plant growth under different abiotic stresses.

Abiotic stress

Plant species

NPs

Positive effects on plants

References

Drought

Wheat

Ti-NP

Increased grain yield and quality

Jaberzadeh et al. (2013)

Drought

Wheat

Analcite

Increased antioxidant activity and reduced ROS production

Zaimenko et al. (2014)

Drought

Maize

Analcite

Increased antioxidant activity and reduced ROS production

Zaimenko et al. (2014)

Drought

Soybean

Zinc NP

Increased seed germination

Sedghi et al. (2013)

Drought

Sunflower Maghemite Reduced drought induced detrimental effects

Martı´nez-Fernandez et al. (2015)

Drought

Safflower

Iron NP

Reduced drought induced detrimental effects

Zareii et al. (2014)

Drought

Basil

Ti-NP

Improved detrimental effects of drought

Kiapour et al. (2015)

Salinity

Tomato

Si-NP

Improved seed germination and seedling establishment

Haghighi et al. (2012)

Salinity

Basil

Si-NP

Increased proline contents and chlorophyll contents

Kalteh et al. (2014)

Salinity

Lentil

Si-NP

Improved seed germination

Sabaghnia and Janmohammadi (2014)

Salinity

Pumpkin

Si-NP

Improved germination, reduced lipid Siddiqui et al. (2014) peroxidation, and increased antioxidant production

Salinity

Sunflower Zinc NP

Improved growth and development, photosynthesis, and chlorophyll fluorescence

Torabian et al. (2016)

Cold

Chickpea

Increased antioxidant activity and reduced electrolytic leakage

Mohammadi et al. (2013, 2014); Hasanpour et al. (2015)

Cold

Arabidopsis Silver NP

Increase expression of antioxidant activity related genes

Kohan-Baghkheirati and Geisler-Lee (2015)

Heat

Tomato

Ti-NP

Enhanced photosynthesis by regulating energy dissipation, caused cooling of leaves through inducing stomatal opening

Qi et al. (2013)

Chromium toxicity

Pea

Na2SiO3

Upregulation of antioxidant defense system and enhanced accumulation of nutrient elements led to improved growth

Tripathi et al. (2015)

Cadmium toxicity

Soybean

Ti-NP

Increased chlorophyll contents, relative water content, and photosynthetic rate

Singh and Lee (2016)

Ti-NP

NP, Nanoparticle; ROS, reactive oxygen species.

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shown that application of Si-NP alleviates arsenic-induced oxidative damage by increasing antioxidant defense system (Tripathi et al., 2015). Similarly, under salt stress, Siddiqui et al. (2014) showed that SiO2-NP enhances salinity tolerance in squash plants via protecting chlorophyll from degradation, improving leaf gas exchange, and also reducing lipid peroxidation and malondialdehyde production. They also reported that SiO2-NP plays a crucial role in increasing different antioxidant enzymes such as SOD, POD, and CAT under salt stress. Plant abiotic stress induce oxidative stress reduce photosynthesis by producing and accumulation ROS in photosynthetic apparatus. Recently, Wu et al. (2017) showed that application of cerium oxide (nCeO2) NP protects CO2 assimilation and quantum yield of photosystem (PS) II by scavenging ROS, induced by different abiotic stresses. Results from other studies showed that nCeO2 reduced hydrogen peroxide production due to its high radical scavenging ability (Xia et al., 2008; Horie et al., 2011). In Medicago arborea, low concentration of nCeO2 improved tolerance to oxidative damage by reducing ROS production in cells (Gomez-Garay et al., 2014). Titanium oxide (TiO2) is another important NP, which can also reduce ROS production and protect plant from oxidative damage. In spinach, nTiO2 considerably reduced hydrogen peroxide and singlet oxygen production in chloroplast under UV-B irradiation (Lei et al., 2008). Similarly in chickpea, nTiO2 application caused tremendous reduction in electrolytic leakage under cold stress and this was due to ability of Ti to oxidize or reduce O22/O2•2 to O2/H2O2 (Mohammadi et al., 2013). In Lemna minor, application of nTiO2 enhanced activity of CAT, glutathione peroxidase (GPOX), and SOD and improved oxidative stress conditions (Song et al., 2012). Nano zinc particles have also been reported as promising plant growth enhancing NPs, for example, nano-ZnO promoted plantlets regeneration, osmotic adjustment, somatic embryogenesis, and antioxidant defense system, thereby enhancing abiotic-stress tolerance (Helaly et al., 2014). According to Wei and Wang (2013), different NPs exhibit antioxidant enzyme-like activities such as nMnO2, nCuO, and nAu exhibit POD like activity; nCeO2, nFe3O4, nCo3O4 have POD and CAT like activities; and nCeO2 and nPt have SOD like property. In conclusion, NPs improves abiotic-stress tolerance in plants by improving antioxidant defense system and by reducing ROS production (Fig. 24.1). Nonetheless exact mechanisms, showing (1) How NPs enhance antioxidant production? (2) Do NPs act as any signaling compound or do they trigger any other signaling compound to activate plant defense system? still have not been identified. Future research should be focused in studying the role of NPs as signaling compounds and abiotic-stress tolerance.

24.4 Nanoparticle application and photosynthetic apparatus CO2 assimilation is a very important mechanism in plants for their survival. Abioticstress conditions alters/reduces this physiological process by disrupting numerous other metabolic processes such as loss of essential nutrient (K1) from leaf mesophyll, degradation of chlorophyll contents, reduced stomatal conductance, and others (Anjum et al., 2016a,c; Tanveer et al., 2018b; Tanveer, 2019). Improving photosynthesis under abioticstress conditions is very important for improving abiotic-stress tolerance in plants. Application of NPs is very attractive approach, which helps in enhancing photosynthesis

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FIGURE 24.1 Toxic effects of nanoparticles on plant growth and development.

in different known and unknown ways. In this section, role of NPs in improving or sustaining photosynthesis under different abiotic conditions has been discussed. Gold NPs (nAu) have been found very promising NPs in improving photosynthesis under abiotic stresses. Govorov and Carmeli (2007) reported that nAu treatment increased photosystem efficiency by improving light absorption by chlorophyll. Similar results have been shown by Barazzouk et al. (2005) and Nieder et al. (2010) that nAu application improves photosynthesis and plant growth. In an in vivo study, soybean treated with nAu NPs showed higher chlorophyll fluoresce (Falco et al., 2011). Role of manganese NPs (nMn) have been examined in photochemistry of Vigna radiata and observed that nMn modulated the activity of PSII by increasing the breakdown of water and release of oxygen and improving the photophosphorylation of ETC (Pradhan et al., 2013). Titanium NPs (nTi) also played crucial role in enhancing photosynthetic activity because of its specific surface area, and high thermal conductivity, and also high photocatalytic ability (Yang et al., 2006; Lei et al., 2007). nTi treatment in spinach chloroplast showed enhanced chlorophyll content, oxygen evolution rate, and electron transfer activities (Lei et al., 2007). In another study, nTi application increased light absorption and conversion in PSII (Qi et al., 2013) and further speculated that electron holes generation in nTi due to enhanced light absorption may trigger release of oxygen from water photolysis and thus increase PSII activity (Lei et al., 2007). Other positive effects of nTi on photosynthetic activity included improved leaf gas exchange and water relation (Qi et al., 2013). Yang et al. (2006) showed that nTi can trigger the activity of ribulose 1,5-bisphosphate carboxylase activity in mesophyll cells and concomitantly increase carbon assimilation. Moreover,

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they also noted that nTi application improves light absorption and protects chloroplast from stress-induced oxidative damage. Partial protection of chloroplast from oxidative damage was found to be associated with enhanced antioxidant activity (Sharma et al., 2012a,b). Furthermore, molecular mechanism, underlying nTi, that induced photosynthesis improvement has been examined and noted that nTi at low concentration increased transcript and protein level for higher Rubisco carboxylation activity. Other than nTi, role of silver NPs and Si-NP has also been examined. Sharma et al. (2012a,b) noted that nAg enhanced light absorption and quantum efficiency of light harvesting in PSII, thus increasing photosynthesis. nSi has been studied as very promising protecting NP that protects numerous physiological processes from oxidation via activating antioxidant defense system. In a study, Tripathi et al. (2015) showed that nSi protected chlorophyll contents and increased photosynthesis by increasing carotenoids contents and antioxidants activity. Moreover, nSi also augments photosynthesis by enhancing carbonic anhydrase enzyme activity and biosynthesis of chlorophyll contents (Siddiqui and Al-Whaibi, 2014) Cesium NPs or nanoceria has been found as the most promising ROS scavengers; nanoceria can scavenge ROS and protect photosynthesis processes under abiotic-stress conditions (Rico et al., 2014). Nanoceria protects and improves carbon and light reaction of photosynthesis by reducing oxidative stress to photosynthetic pigments, membranes, lipids, and enzymes involved in photosynthesis (Deshpande et al., 2005; Tarnuzzer et al., 2005). Nanoceria can scavenge different ROS such as H2O2, OH2, and O22 and triggered their conversion into oxygen, hydroxyl radical, and water (Xue et al., 2011; Gupta et al., 2016). Nanoceria can protect the chloroplasts from ROS damages and improved its photosynthetic activity (Boghossian et al., 2013; Giraldo et al., 2014). In conclusion, NPs application significantly improves plant growth via increasing photosynthesis and photosynthesis contributing traits (Fig. 24.1).

24.5 Nanoparticles application and ionic homeostasis Abiotic stresses along with inducing oxidative stress also causes ionic stress, defined as excess accumulation of essential or nonessential ions or toxic heavy metal in plant cells that can significantly disrupt plant normal metabolism under normal growth conditions. Under different heavy metal stresses, accumulation of toxic heavy metal ions leads to significant reduction in plant growth and yield (Anjum et al., 2016a,b, 2017d). These toxic ions primarily cause cytosolic toxicity and disrupt a number of physiological processes such as nutrient transport, signaling, and/or photosynthesis (Shahzad et al., 2016). Furthermore, different abiotic stresses alter ionic homeostasis in plant cells either by reducing their uptake or by replacing them. For example, under salt stress, Na1 replaces K1 or Ca21. Therefore it is important to reduce either toxic ion uptake or improve ability of plant to avoid cytosolic toxicity (Tanveer et al., 2018a). Nanotechnology or application of NPs is found very promising in alleviating ionic stress caused by different abiotic factors. These NPs can reduce accumulation of toxic ions in cells and protect plants from ionic stress. Because of their smaller size and large surface area, these engineered NPs have found as highly effective in ameliorating heavy metal-induced toxic effects in plants

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(Gunjan et al., 2014). Primarily, these NPs can easily bind to metal ions and reduce their availability. For instance, quantum dots can reduce the availability of lead and copper and limit the entry of these toxic ions via roots (Worms et al., 2012). On other hand, if heavy metals enter the plant cells and causes oxidative damage or ionic toxicity, these NPs triggers plant defense system and increase accumulation of some important ions such as K1 or Ca21. Role of nTi has been extensively studied in this regard. nTi restricts the entry of cadmium and enhances carbon-assimilation process in plants (Singh and Lee, 2016). Hydroxyapatite also reduces cadmium uptake and toxicity in Brassica chinensis by increasing antioxidant production and chlorophyll contents (Li and Huang, 2014). Furthermore, nFe application increased microbial activity, which reduced Cr bioavailability (Madhavi et al., 2013). In a study, application of Si-NPs was showed to have ameliorating effects on Cr induced toxic effects in plants (Tripathi et al., 2015). Application of zero valent iron NPs is found as potential approach to reduce uranium toxicity (Dickinson and Scott, 2010). Moreover, Shabnam et al. (2014) observed that nAu application reduces Al toxicity in cowpea. In conclusion, application of NPs is a very promising approach which reduces heavy metal toxicity via reducing heavy metal ion accumulation and by improving plant growth. Salt stress is another abiotic stress, which causes ionic toxicity and disrupts ionic homeostasis (Tanveer and Shabala, 2018). Under salt stress, high accumulation of Na1 or Cl2 ions in plant cell causes cellular ionic toxicity (Shabala et al., 2015; Tanveer and Shah, 2017). In plants, salt stress significantly induces the efflux of K1 from leaf mesophyll cells and increases Na1 accumulation in cytosol (Shabala and Cuin, 2008). NPs application can ameliorate salt stress by reducing salt stress induced toxic effects. For example, Si significantly ameliorates salt stress and increases seed germination, antioxidant defense system, leaf turgor, and carbon-assimilation process (Haghighi and Pessarakli, 2013; Qados, 2015). In tomato, application of nano-Si significantly alleviates salt stress by reducing Na1 toxicity and ROS production (Haghighi et al., 2012). Similar effects of nSi have been examined in different other crop plants such as basil, lentil, and broad bean (Sabaghnia and Janmohammadi, 2014; Qados, 2015).

24.6 Nanoparticles toxicity in plants Literature shows that metallic NPs fall into two major categories, namely, pure metals and metal oxides. NPs induce both positive and negative effects on seed germination, root/shoot growth, biomass accumulation, and biochemical/physiological processes under NPs; however, toxicological impacts are more pronounced than their beneficial effects on plants (Table 24.2) (Mohamed and Kumar, 2016). Higher concentrations of NPs pose serious consequences on plants by changing morphophysiological, anatomical, and genetic traits (Fig. 24.1) (Rico et al., 2015; Tripathi et al., 2015). Nonetheless, the extent of NPs toxicity on plant growth and metabolism highly depends on several factors such as size, concentration, and chemistry of NPs as well as exposure to NPs (Dietz and Herth, 2011). At higher concentrations, NPs cause inhibition in the development of seedling and roots (Wang et al., 2012). This is also evident from Burklew et al. (2012) who showed that reduced growth and development of tobacco plants was exhibited under NPs.

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TABLE 24.2 Reported examples of toxic effects of different nanoparticles (NP) in plants. Plant species

NP

NP size (nm)

Onion

Fullerol

Onion

NP concentration

Toxic effects in plants

References

18.17 24.36 110 mg/L

Oxidative damage and necrosis

Chen et al. (2010)

Silver NP

, 100

100 ppm

Disturbed mitosis and breakdown of cell wall

Kumari et al. (2009)

Rice

Single walled carbon NP

1 2

25 mg/L

H2O2 production, DNA damage and enhanced chromatin condensation

Shen et al. (2010)

Red spinach

Multi-walled carbon NP

10

125 1000 mg/L Reduced stomatal conductance, and ROS production

Spinach

Titanium NP

5

0.25%

Limited photosynthetic rate due to Lei et al. (2008) oxidative damage to chloroplast

Arabidopsis Silver NP

20

5 25 mg/L

Oxidative stress and down regulation of genes linked with ethylene production

Kaveh et al. (2013)

Squash

Silver NP

, 100

500 mg/L

Declined transpiration

Musante and White (2012)

Pea

Zinc NP

10

500 ppm

ROS and RNS production and degradation of chlorophyll

Mukherjee et al. (2014)

Tobacco

Aluminum NP

, 50

100 ppm

ROS production and enhanced lipid peroxidation

Poborilova et al. (2013)

Brassica

Gold NP

10 20

100 ppm

Imbalanced hormone production and oxidative damage

Arora et al. (2012)

Squash

Copper NP

, 50

500 mg/L

Reduced transpiration

Musante and White (2012)

Begum and Fugetsu (2012)

ROS, Reactive oxygen species.

Essentiality of Cu is inevitable. Being a vital element, it plays numerous important roles in acclimation of plant growth and development including photosynthesis, RNA biosynthesis, and activation of several enzymes leading to improved performance of photosystem I and II (Leng et al., 2015). However, higher concentration of Cu oxide NPs showed negative influences on plant growth and development in terms of seed germination and seedling growth (Sethy and Ghosh, 2013). Several studies have demonstrated toxicity of nCu which caused oxidative damage to cellular structures as well as necrosis and chlorotic symptoms can be seen under the influence of ROS (Yruela, 2005; Xiong and Wang, 2005; Manceau et al., 2008). Atha et al. (2012) showed that nCu negatively affected the root and shoot growth of perennial ryegrass (Lolium perenne L.). Similarly, nCu treatment caused 50% reduction in growth of duckweed (Landoltia punctata) (Shi et al., 2011). Studies on the adverse effects of NPs on plants must be implemented as it is a common practice to utilize NPs as nanofertilizers and nanopesticides in agriculture sector (Selivanov and Zorin, 2001;

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Raikova et al., 2006). It is evident from the investigation of Adhikari et al. (2012) that nCu have least toxic effect on seed germination of Cicer arietinum L. and Glycine max L. that is because of the seed coat that protected the embryo inside the seed. However, dose dependent decrease in root elongation and primary root development was associated with NPs toxicity. Hence, presence of dispersed nCu as environmental contaminants may have several detrimental health-related issues and toxicological effects on other living organisms including plants and making it a threat to living organism and challenge for researcher (Adhikari et al., 2012; Aruoja et al., 2009; Chang et al., 2012). Several other studies have shown negative effects of NPs on plant growth and development as well. For instance, nCu substantially reduced morphological parameters and decreased net photosynthesis (gas exchange parameters) with an overall negative impact on antioxidant enzymes activity (Da Costa and Sharma, 2016). Authors further illustrated the toxicity of nCu, that is, treating with high concentration (1000 mg/L) of nCu resulted in reduced germination rate, fresh biomass accumulation, and number of thylakoids per granum in chloroplasts as well as caused complete loss of quenching capacity of photosystem II (Da Costa and Sharma, 2016). Hong et al. (2016) showed that nCu altered the normal physiological parameters, nutrient contents, and antioxidant enzyme activity in both lettuce (Lactuca sativa) and alfalfa (Medicago sativa) plants. Similarly, nCu decreased ascorbic acid and amino acid contents such as oxoproline, proline, arginine, ornithine, leucine, serine, and tyrosine (Olkhovych et al., 2016). There are few other studies showing reduced biomass yield in potato (Bradfield et al., 2017) and carrot (Ebbs et al., 2016), diminished nutrient acquisition, and increased expression of Bt toxin protein in cotton leading to stunted growth of cotton plants (Le Van et al., 2016). It is now well established fact that NPs affect the plant development and metabolism, but the extent of its toxicity highly depends on size, concentration, chemistry, and NPs type (Dietz and Herth, 2011). Assessing the risk associated with the release of NPs in the environment requires a better understanding that how these NPs are likely to link with the release, transport, bioavailability, and its fate in an ecosystem. It is also evident that the extent of NPs toxicity is not the same for different plants, and it varies from species to species. Some plants do not show any toxicity symptoms although significant variation exists in the upregulation of antioxidant activity (Siddiqi and Husen, 2016). In a study, Shabnam et al. (2014) showed that application of HAuCl4 NPs did not alter the physiological traits of cow pea and showed no visible influence on growth and biomass accumulation even 1 mM concentration of NPs were detected in the plants. Lin and Xing (2008) tested effect of five different NPs on the germination and seedling vigor of important agricultural crops (ryegrass, corn, rape, cucumber, lettuce, and radish) and observed that different types of NPs did not affect the seed germination; however, ryegrass and corn showed reduced germination rate. Moreover, they found that nZn induced more detrimental effects on seed germination and root growth than other NPs (Al, Cu, and C). Interestingly, Al2O3 NPs reduced the root length of plants, which was linked with aluminum NPs despite the fact that soluble aluminum itself is a potent toxicant to the roots. It is in line with another study under coated and uncoated aluminum NPs in hydroponics where uncoated NPs decreased root elongation but not with the coated one (Yang and Watts, 2005). Therefore it is proposed that surface properties of NPs are an important indicator in characterizing NPs toxicities under exposure to different NPs. While Lin and Xing recommended that some plant seeds

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could be more resistant to applied NPs and/or their seed coat may hinder the entry of NPs. Another important notion could be the involvement of their antioxidant defense system (enzymatic and nonenzymatic antioxidants) to prevent the oxidative damage under NPs stress (Kumari et al., 2017). Toxic effects of NPs may differ from plant to plant. Therefore exact mechanism underlying plant defense system against the NPs induced toxicity is still unclear. Moreover, absorption and translocation of NPs in different plant parts is highly dependable on concentration, bioavailability, and exposure time.

24.7 Conclusion Prevalence of abiotic stresses is inevitable under current climate change conditions. Furthermore, modern agriculture further kindled the situation by deteriorating natural resources. In such situation, improving abiotic-stress tolerance in plants is very much imperative to enhance agricultural productivity. Nanotechnology is found as most promising approach to improve abiotic-stress tolerance. Research conducted so far on NPs application and abiotic-stress tolerance showed that NPs increase abiotic-stress tolerance majorly by scavenging ROS and by enhancing photosynthesis. However, contradictions are still there, which showed NPs especially metallic NPs or metallic oxide NPs are toxic to plants. Positive or negative effects of NPs depend on numerous factors such as their concentration, surface charge, surface area, and exposure regime. Future research should be focused to investigate positive effects of NPs on other traits such as osmolytes accumulation or ionic homeostasis under abiotic stresses.

References Adhikari, T., Kundu, S., Biswas, A.K., Tarafdar, J.C., Rao, A.S., 2012. Effect of copper oxide nano particle on seed germination of selected crops. J. Agric. Sci. Technol. 2 (6A), 815. Adrees, M., Ali, S., Rizwan, M., Ibrahim, M., Abbas, F., Farid, M., et al., 2015. The effect of excess copper on growth and physiology of important food crops: a review. Environ. Sci. Pollut. Res. 22 (11), 8148 8162. Anjum, S.A., Ashraf, U., Khan, I., Tanveer, M., Saleem, M.F., Wang, L., 2016a. Aluminum and chromium toxicity in maize: implications for agronomic attributes, net photosynthesis, physio-biochemical oscillations, and metal accumulation in different plant parts. Water Air Soil Pollut. 227 (9), 326. Anjum, S.A., Ashraf, U., Khan, I., Tanveer, M., Ali, M., Hussain, I., et al., 2016b. Chromium and aluminum phytotoxicity in maize: morpho-physiological responses and metal uptake. CLEAN—Soil Air Water 44 (8), 1075 1084. Anjum, S.A., Tanveer, M., Ashraf, U., Hussain, S., Shahzad, B., Khan, I., et al., 2016c. Effect of progressive drought stress on growth, leaf gas exchange, and antioxidant production in two maize cultivars. Environ. Sci. Pollut. Res 23 (17), 17132 17141. Anjum, S.A., Ashraf, U., Imran, K., Tanveer, M., Shahid, M., Shakoor, A., et al., 2017a. Phyto-toxicity of chromium in maize: oxidative damage, osmolyte accumulation, anti-oxidative defense and chromium uptake. Pedosphere 27 (2), 262 273. Anjum, S.A., Ashraf, U., Tanveer, M., Khan, I., Hussain, S., Shahzad, B., et al., 2017b. Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front. Plant Sci. 8 (69). Available from: https://doi.org/10.3389/fpls.2017.00069. Anjum, S.A., Ashraf, U., Zohaib, A., Tanveer, M., Naeem, M., Iftikhar, A.L.I., et al., 2017c. Growth and developmental responses of crop plants under drought stress: a review. Zemdirbyste-Agric. 104, 267 276.

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References

637

Anjum, S.A., Tanveer, M., Hussain, S., Ashraf, U., Khan, I., Wang, L., 2017d. Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress. Water Air Soil Pollut. 228 (1), 13. Arora, S., Sharma, P., Kumar, S., Nayan, R., Khanna, P.K., Zaidi, M.G.H., 2012. Gold- nanoparticle induced enhancement in growth and seed yield of Brassica juncea. Plant Growth Regul. 66 (3), 303 310. Aruoja, V., Dubourguier, H.-C., Kasemets, K., Kahru, A., 2009. Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci. Total Environ. 407, 1461 1468. Atha, D.H., Wang, H., Petersen, E.J., Cleveland, D., Holbrook, R.D., Jaruga, P., et al., 2012. Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environ. Sci. Technol. 46, 1819 1827. Barazzouk, S., Kamat, P.V., Hotchandani, S., 2005. Photoinduced electron transfer between chlorophyll a and gold nanoparticles. J. Phys. Chem. B. 109, 716 723. Begum, P., Fugetsu, B., 2012. Phytotoxicity of multi-walled carbon nanotubes on red spinach (Amaranthus tricolor L.) and the role of ascorbic acid as an antioxidant. J. Hazard. Mater. 243, 212 222. Boghossian, A.A., Sen, F., Gibbons, B.M., Sen, S., Faltermeier, S.M., Giraldo, J.P., et al., 2013. Application of nanoparticle antioxidants to enable hyperstable chloroplasts for solar energy harvesting. Adv. Energy Mater. 3, 881 893. Bradfield, S.J., Kumar, P., White, J.C., Ebbs, S.D., 2017. Zinc, copper, or cerium accumulation from metal oxide nanoparticles or ions in sweet potato: yield effects and projected dietary intake from consumption. Plant Physiol. Biochem. 110, 128 137. Burklew, C.E., Ashlock, J., Winfrey, W.B., Zhang, B., 2012. Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotianatabacum). PLoS One 7, 734 783. Available from: https://doi.org/10.1371/journal.pone.0034783. Chang, Y.N., Zhang, M., Xia, L., Zhang, J., Xing, G., 2012. The toxic effects and mechanisms of CuO and ZnO nanoparticles. Materials 5 (12), 2850 2871. Chen, R., Ratnikova, T.A., Stone, M.B., Lin, S., Lard, M., Huang, G., et al., 2010. Differential uptake of carbon nanoparticles by plant and mammalian cells. Small 6 (5), 612 617. Da Costa, M.V.J., Sharma, P.K., 2016. Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica 54 (1), 110 119. Demidchik, V., 2015. Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ. Exp. Bot. 109, 212 228. Deshpande, S., Patil, S., Kuchibhatla, S.V., Seal, S., 2005. Size dependency variation in lattice parameter and valency states in nanocrystalline cerium oxide. Appl. Phys. Lett. 87, 133113. Dickinson, M., Scott, T.B., 2010. The application of zero-valent iron nanoparticles for the remediation of a uranium contaminated waste effluent. J. Hazard. Mater. 178, 171 179. Dietz, K.J., Herth, S., 2011. Plant nanotoxicology. Trends Plant Sci. 16 (11), 582 589. Ebbs, S.D., Bradfield, S.J., Kumar, P., White, J.C., Musante, C., Ma, X., 2016. Accumulation of zinc, copper, or cerium in carrot (Daucus carota) exposed to metal oxide nanoparticles and metal ions. Environ. Sci. 3, 114 126. Falco, W.F., Botero, E.R., Falcao, E.A., et al., 2011. In vivo observation of chlorophyll fluorescence quenching induced by gold nanoparticles. J. Photochem. Photobiol. A 225, 65 71. Giraldo, J.P., Landry, M.P., Faltermeier, S.M., McNicholas, T.P., Iverson, N.M., Boghossian, A.A., et al., 2014. Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat. Mater. 13, 400 408. Gomez-Garay, A., Pintos, B., Manzanera, J.A., Lobo, C., Villalobos, N., Martı´n, L., 2014. Uptake of CeO2 nanoparticles and its effect on growth of Medicago arborea in vitro plantlets. Biol. Trace Elem. Res. Available from: https://doi.org/10.1007/s12011-014-0089-2. Govorov, A.O., Carmeli, I., 2007. Hybrid structures composed of photosynthetic system and metal nanoparticles: plasmon enhancement effect. Nano letters 7 (3), 620 625. Gunjan, B., Zaidi, M.G.H., Sandeep, A., 2014. Impact of gold nanoparticles on physiological and biochemical characteristics of Brassica juncea. J. Plant Biochem. Physiol. 2, 133. Available from: https://doi.org/10.4172/23299029.1000133. Gupta, A., Das, S., Neal, C.J., Seal, S., 2016. Controlling the surface chemistry of cerium oxide nanoparticles for biological applications. J. Mater. Chem. B 4, 3195 3202. Haghighi, M., Pessarakli, M., 2013. Influence of silicon and nano-silicon on salinity tolerance of cherry tomatoes (Solanum lycopersicum L.) at early growth stage. Sci. Hortic. 161, 111 117.

Plant Life under Changing Environment

638

24. Nanoparticle application and abiotic-stress tolerance in plants

Haghighi, M., Afifipour, Z., Mozafarian, M., 2012. The effect of N-Si on tomato seed germination under salinity levels. J. Biol. Environ. Sci. 6, 87 90. Hasanpour, H., Maali-Amiri, R., Zeinali, H., 2015. Effect of TiO2 nanoparticles on metabolic limitations to photosynthesis under cold in chickpea. Russ. J. Plant Physiol. 62, 779 787. Helaly, M.N., El-Metwally, M.A., El-Hoseiny, H., Omar, S.A., El-Sheery, N.I., 2014. Effect of nanoparticles on biological contamination of in vitro cultures and organogenic regeneration of banana. Aust. J. Crop Sci. 8, 612 624. Hong, J., Rico, C.M., Zhao, L., Adeleye, A.S., Keller, A.A., Peralta-Videa, J.R., et al., 2016. Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa). Environ. Sci. 17, 177 185. Horie, M., Nishio, K., Kato, H., Fujita, K., Endoh, S., Nakamura, A., et al., 2011. Cellular responses induced by cerium oxide nanoparticles: induction of intracellular calcium level and oxidative stress on culture cells. J. Biochem. 150, 461 471. Hussain, M., Farooq, S., Hasan, W., Ul-Allah, S., Tanveer, M., Farooq, M., et al., 2018. Drought stress in sunflower: physiological effects and its management through breeding and agronomic alternatives. Agric. Water Manage. 201, 152 166. Jaberzadeh, A., Moaveni, P., Reza, H., Moghadam, T., Zahedi, H., 2013. Influence of bulk and nanoparticles titanium foliar application on some agronomic traits, seed gluten and starch contents of wheat subjected to water deficit stress. Not. Bot. Horti Agrobo. 41, 201 207. Kalteh, M., Alipour, Z.T., Ashraf, S., Aliabadi, M.M., Nosratabadi, A.F., 2014. Effect of silica nanoparticles on basil (Ocimum basilicum) under salinity stress. J. Chem. Health Risks 4, 49 55. Kaveh, R., Li, Y.S., Ranjbar, S., Tehrani, R., Brueck, C.L., Van Aken, B., 2013. Changes in Arabidopsis thaliana gene expression in response to silver nanoparticles and silver ions. Environ. Sci. Technol. 47 (18), 10637 10644. Khan, F., Hussain, S., Tanveer, M., Khan, S., Hussain, H.A., Iqbal, B., et al., 2018. Coordinated effects of lead toxicity and nutrient deprivation on growth, oxidative status, and elemental composition of primed and nonprimed rice seedlings. Environ. Sci. Pollut. Res. Available from: https://doi.org/10.1007/s11356-018-2262-1. Kiapour, H., Moaveni, P., Habibi, D., Sani, B., 2015. Evaluation of the application of gibbrellic acid and titanium dioxide nanoparticles under drought stress on some traits of basil (Ocimum basilicum L.). Int. J. Agron. Agric. Res. 6, 138 150. Kohan-Baghkheirati, E., Geisler-Lee, J., 2015. Gene expression, protein function and pathways of Arabidopsis thaliana responding to silver nanoparticles in comparison to silver ions, cold, salt, drought, and heat. Nanomaterials 5, 436 467. Krzesłowska, M., 2011. The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol. Plant. 33 (1), 35 51. Kumari, M., Mukherjee, A., Chandrasekaran, N., 2009. Genotoxicity of silver nanoparticles in Allium cepa. Sci. Total Environ. 407 (19), 5243 5246. Kumari, R., Singh, J.S., Singh, D.P., 2017. Biogenic synthesis and spatial distribution of silver nanoparticles in the legume mung bean plant (Vigna radiata L.). Plant Physiol. Biochem. 110, 158 166. Available from: https://doi. org/10.1016/j.plaphy.2016.06.001. Le Van, N., Ma, C., Shang, J., Rui, Y., Liu, S., Xing, B., 2016. Effects of CuO nanoparticles on insecticidal activity and phytotoxicity in conventional and transgenic cotton. Chemosphere 144, 661 670. Lei, Z., Mingyu, S., Chao, L., Liang, C., Hao, H., Xiao, W., et al., 2007. Effects of nanoanatase TiO2 on photosynthesis of spinach chloroplasts under different light illumination. Biol. Trace Elem. Res. 119 (1), 68 76. Lei, Z., Mingyu, S., Xiao, W., Chao, L., Chunxiang, Q., Liang, C., et al., 2008. Antioxidant stress is promoted by nano-anatase in spinach chloroplasts under UV-B radiation. Biol. Trace Elem. Res. 121 (1), 69 79. Leng, X., Jia, H., Sun, X., Shangguan, L., Mu, Q., Wang, B., et al., 2015. Comparative transcriptome analysis of grapevine in response to copper stress. Nat. Publ. Group Sci. Rep. 5, 17749. Li, Z., Huang, J., 2014. Effects of nanoparticle hydroxyapatite on growth and antioxidant system in pak choi (Brassica chinensis L.) from cadmium-contaminated soil. J. Nanomater. 2014, 1 7. Lin, D., Xing, B., 2008. Root uptake and phytotoxicity of ZnO nanoparticles. Environ. Sci. Tech. 42 (15), 5580 5585. Madhavi, V., Prasad, T., Reddy, A.V.B., Madhavi, G., 2013. Plant growth promoting potential of nanobioremediation under Cr(VI) stress. Int. J. Nanotechnol. Appl. 3, 1 10. Manceau, A., Nagy, K.L., Marcus, M.A., Lanson, M., Geoffroy, N., Jacquet, T., et al., 2008. Formation of metallic copper nanoparticles at the soil root interface. Environ. Sci. Technol. 42 (5), 1766 1772.

Plant Life under Changing Environment

References

639

Martı´nez-Fernandez, D., Vı´tkova, M., Bernal, M.P., Komarek, M., 2015. Effects of nano-maghemite on trace element accumulation and drought response of Helianthus annuus L. in a contaminated mine soil. Water Air Soil Pollut. 226, 101. Available from: https://doi.org/10.1007/s11270-015-2365-y. Mohamed, M.S., Kumar, D.S., 2016. Effect of nanoparticles on plants with regard to physiological attributes. Plant Nanotechnology. Springer, pp. 119 153. Available from: https://doi.org.10.1007/978-3-319-42154-4_6. Mohammadi, R., Maali-Amiri, R., Abbasi, A., 2013. Effect of TiO2 nanoparticles on chickpea response to cold stress. Biol. Trace Elem. Res. Available from: https://doi.org/10.1007/s12011-013-9631-x. Moisala, A., Nasibulin, A.G., Kauppinen, E.I., 2003. The role of metal nanoparticles in the catalytic production of single-walled carbon nanotubes—a review. J. Phys.: Condens. Matter 15, 03 11. Monica, R.C., Cremonini, R., 2009. Nanoparticles and higher plants. Caryologia 62 (2), 161 165. Mukherjee, A., Peralta-Videa, J.R., Bandyopadhyay, S., Rico, C.M., Zhao, L., Gardea-Torresdey, J.L., 2014. Physiological effects of nanoparticulate ZnO in green peas (Pisum sativum L.) cultivated in soil. Metallomics 6, 132 138. Available from: https://doi.org/10.1039/c3mt00064h. Musante, C., White, J.C., 2012. Toxicity of silver and copper to Cucurbita pepo: differential effects of nano and bulk- size particles. Environ. Toxicol. 27 (9), 510 517. Nekrasova, G.F., Ushakova, O.S., Ermakov, A.E., Uimin, M.A., Byzov, I.V., 2011. Effects of copper (II) ions and copper oxide nanoparticles on Elodea densa Planch. Russ. J. Ecol. 42 (6), 458 463. Nieder, J.B., Bittl, R., Brecht, M., 2010. Fluorescence studies into the effect of plasmonic interactions on protein function. Angew. Chem. Int. Ed. 49, 10217 10220. Olkhovych, O., Volkogon, M., Taran, N., Batsmanova, L., Kravchenko, I., 2016. The effect of copper and zinc nanoparticles on the growth parameters, contents of ascorbic acid, and qualitative composition of amino acids and acylcarnitines in Pistia stratiotes L. (Araceae). Nanoscale Res. Lett. 11, 218. Pradhan, S., Patra, P., Das, S., et al., 2013. Photochemical modulation of biosafe manganese nanoparticles on Vigna radiata: a detailed molecular, biochemical, and biophysical study. Environ. Sci. Technol. 47, 13122 13131. Poborilova, Z., Opatrilova, R., Babula, P., 2013. Toxicity of aluminium oxide nanoparticles demonstrated using a BY-2 plant cell suspension culture model. Environ. Exp. Bot. 91, 1 11. Qados, A.M.S.A., 2015. Mechanism of nanosilicon-mediated alleviation of salinity stress in faba bean (Vicia faba L.) plants. Am. J. Exp. Agric. 7 (78), e95. Qi, M., Liu, Y., Li, T., 2013. Nano-TiO2 improve the photosynthesis of tomato leaves under mild heat stress. Biol. Trace Elem. Res. 156 (323), e328. Raikova, O.P., Panichkin, L.A., Raikova, N.N., 2006. Studies on the effect of ultrafine metal powders produced by different methods on plant growth and development. Nanotechnologies and information technologies in the 21st century. In: Proceedings of the International Scientific and Practical Conference, pp. 108 111. Rico, C.M., Lee, S.C., Rubenecia, R., Mukherjee, A., Hong, J., Peralta-Videa, J.R., et al., 2014. Cerium Oxide Nanoparticles Impact Yield and Modify Nutritional Parameters in Wheat (Triticum aestivum L.). J. Agric. Food. Chem. 62, 9669 9675. Rico, C.M., Peralta-Videa, J.R., Garadea-Torresdey, J.L., 2015. Chemistry, biochemistry of nanoparticles, and their role in antioxidant defense system in plants. In: Siddiqui, H.M., et al., (Eds.), Nanotechnology and Plant Sciences. Springer International Publishing, Switzerland, pp. 1 17. Sabaghnia, N., Janmohammadi, M., 2014. Effect of nanosilicon particles application on salinity tolerance in early growth of some lentil genotypes. Ann. UMCS Biol. 69, 39 55. Sedghi, M., Hadi, M., Toluie, S.G., 2013. Effect of nano zinc oxide on the germination parameters of soybean seeds under drought stress. Ann. West Univ. Timisoara Ser. Biol. 16, 73 78. Selivanov, V.N., Zorin, E.V., 2001. Sustained action of ultrafine metal powders on seeds of grain crops. Perspect. Mater. 4, 66 69. Sethy, S.K., Ghosh, S., 2013. Effect of heavy metals on germination of seeds. J. Nat. Sci. Biol. Med. 4 (2), 272 275. Shabala, S., Cuin, T.A., 2008. Potassium transport and plant salt tolerance. Physiol. Plant. 133 (4), 651 669. Shabala, S., Wu, H., Bose, J., 2015. Salt stress sensing and early signaling events in plant roots: current knowledge and hypothesis. Plant Sci. 241, 109 119. Shabnam, N., Pardha-Saradhi, P., Sharmila, P., 2014. Phenolics impart Au3 þ-stress tolerance to cowpea by generating nanoparticles. PLoS One 9, 85242.

Plant Life under Changing Environment

640

24. Nanoparticle application and abiotic-stress tolerance in plants

Shahzad, B., Tanveer, M., Hassan, W., Shah, A.N., Anjum, S.A., Cheema, S.A., et al., 2016. Lithium toxicity in plants: reasons, mechanisms and remediation possibilities—a review. Plant Physiol. Biochem. 107, 104 115. Available from: https://doi.org/10.1016/j.plaphy.2016.05.034. Shahzad, B., Tanveer, M., Che, Z., Rehman, A., Cheema, S.A., Sharma, A., et al., 2018. Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review. Ecotoxicol. Environ. Saf. 147, 935 944. Shao, H.B., Chu, L.Y., Shao, M.A., Jaleel, C.A., Hong-mei, M., 2008. Higher plant antioxidants and redox signaling under environmental stresses. Comptes Rendus Biol 331, 433 441. Sharma, P., Bhatt, D., Zaidi, M.G.H., et al., 2012a. Silver nanoparticle-mediated enhancement in growth and antioxidant status of Brassica juncea. Appl. Biochem. Biotechnol. 167, 2225 2233. Sharma, P., Jha, A.B., Dubey, R.S., Pessarakli, M., 2012b. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot. Available from: https://doi.org/ 10.1155/2012/217037. Shaw, A.K., Hossain, Z., 2013. Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere 93 (6), 906 915. Shen, C.X., Zhang, Q.F., Li, J., Bi, F.C., Yao, N., 2010. Induction of programmed cell death in Arabidopsis and rice by single-wall carbon nanotubes. Am. J. Bot. 97 (10), 1602 1609. Shi, J., Abid, A.D., Kennedy, I.M., Hristova, K.R., Silk, W.K., 2011. To duckweeds (Landoltia punctata), nanoparticulate copper oxide is more inhibitory than the soluble copper in the bulk solution. Environ. Pollut. 159 (5), 1277 1282. Siddiqi, K.S., Husen, A., 2016. Engineered gold nanoparticles and plant adaptation potential. Nanoscale Res. Lett. 11, 400. Available from: https://doi.org/10.1186/s11671-016-1607-2. Siddiqui, M.H., Al-Whaibi, M.H., 2014. Role of nano-SiO2 in germination of tomato (Lycopersicum esculentum Mill.) seeds. Saudi J. Biol. Sci. 21, 13 17. Siddiqui, M.H., Al-Whaibi, M.H., Faisal, M., Al Sahli, A.A., 2014. Nano-silicon dioxide mitigates the adverse effects of salt stress on Cucurbita pepo L. Environ. Toxicol. Chem 33 (11), 2429 2437. Singh, J., Lee, B.K., 2016. Influence of nano-TiO2 particles on the bioaccumulation of Cd in soybean plants (Glycine max): a possible mechanism for the removal of Cd from the contaminated soil. J. Environ. Manage. 170, 88 96. Song, G., Gao, Y., Wu, H., Hou, W., Zhang, C., Ma, H., 2012. Physiological effect of anatase TiO2 nanoparticles on Lemna minor. Environ. Toxicol. Chem. 31, 2147 2152. Tanveer, M., 2019. Role of 24-epibrassinolide in inducing thermo-tolerance in plants. J. Plant Growth Regul. Available from: https://doi.org/10.1007/s00344-018-9904-x. Tanveer, M., Shabala, S., 2018. Targeting redox regulatory mechanisms for salinity stress tolerance in Crops, Salinity Responses and Tolerance in Plants, Volume 1. Springer, Cham, pp. 213 234. Tanveer, M., Shah, A.N., 2017. An insight into salt stress tolerance mechanisms of Chenopodium album. Environ. Sci. Pollut. Res. 24, 16531 16535. Tanveer, M., Shahzad, B., Sharma, A., Biju, S., Bhardwaj, R., 2018a. 24-Epibrassinolide; an active brassinolide and its role in salt stress tolerance in plants: a review. Plant Physiol. Biochem. 130, 69 79. Tanveer, M., Shahzad, B., Sharma, A., Khan, E.A., 2018b. 24-Epibrassinolide application in plants: an implication for improving drought stress tolerance in plants. Plant Physiol. Biochem. 135, 295 303. Tarnuzzer, R.W., Colon, J., Patil, S., Seal, S., 2005. Vacancy engineered ceria nanostructures for protection from radiation-induced cellular damage. Nano Lett. 5, 2573 2577. Torabian, S., Zahedi, M., Khoshgoftar, A.H., 2016. Effects of foliar spray of two kinds of zinc oxide on the growth and ion concentration of sunflower cultivars under salt stress. J. Plant Nutr. 39, 172 180. Tripathi, D.K., Singh, V.P., Prasad, S.M., Chauhan, D.K., Dubey, N.K., 2015. Silicon nanoparticles (SiNp) alleviate chromium(VI) phytotoxicity in Pisum sativum (L.) seedlings. Plant Physiol. Biochem. 96, 189 198. Available from: https://doi.org/10.1016/j.plaphy.2015.07.026. Wang, Q., Ma, X., Zhang, W., Pei, H., Chen, Y., 2012. The impact of cerium oxide nanoparticles on tomato (Solanum lycopersicum L.) and its implications for food safety. Metallomics 4, 1105 1112. Available from: https://doi.org/10.1039/c2mt20149f. Wei, H., Wang, E., 2013. Nanomaterials with enzyme-like characteristics (nanozymes): next-generation artificial enzymes. Chem. Soc. Rev. 42, 6060 6093.

Plant Life under Changing Environment

Further reading

641

Worms, I.A.M., Boltzman, J., Garcia, M., Slaveykova, V.I., 2012. Cell-wall-dependent effect of carboxyl-CdSe/ZnS quantum dots on lead and copper availability to green microalgae. Environ. Pollut. 167, 27 33. Wu, H., Tito, N., Giraldo, J.P., 2017. Anionic cerium oxide nanoparticles protect plant photosynthesis from abiotic stress by scavenging reactive oxygen species. ACS Nano 11 (11), 11283 11297. Xia, T., Kovochich, M., Liong, M., Ma¨dler, L., Gilbert, B., Shi, H., et al., 2008. Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2, 2121 2134. Xiong, Z.T., Wang, H., 2005. Copper toxicity and bioaccumulation in Chinese cabbage (Brassica pekinensis Rupr.). Environ. Toxicol. 20 (2), 188 194. Xue, Y., Luan, Q., Yang, D., Yao, X., Zhou, K., 2011. Direct evidence for hydroxyl radical scavenging activity of cerium oxide nanoparticles. J. Phys. Chem. C 115, 4433 4438. Yang, L., Watts, D.J., 2005. Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicol. Lett. 158, 122 132. Yang, F., Hong, F.S., You, W.J., Liu, C., Gao, F.Q., Wu, C., et al., 2006. Influences of nano-anatase TiO2 on the nitrogen metabolism of growing spinach. Biol. Trace Elem. Res. 110, 179 190. Yruela, I., 2005. Copper in plants. Braz. J. Plant Physiol. (Lond.) 17 (1), 145 156. Zaimenko, N.V., Didyk, N.P., Dzyuba, O.I., Zakrasov, O.V., Rositska, N.V., Viter, A.V., 2014. Enhancement of drought resistance in wheat and corn by nanoparticles of natural mineral analcite. Ecol. Balk. 6, 1 10. Zareii, F.D., Roozbahani, A., Hosnamidi, A., 2014. Evaluation the effect of water stress and foliar application of Fe nanoparticles on yield, yield components and oil percentage of safflower (Carthamus tinctorius L.). Int. J. Adv. Biol. Biomed. Res. 2, 1150 1159.

Further reading Iannone, M.F., Groppa, M.D., de Sousa, M.E., van Raap, M.B.F., Benavides, M.P., 2016a. Impact of magnetite iron oxide nanoparticles on wheat (Triticum aestivum L.) development: evaluation of oxidative damage. Environ. Exp. Bot. 131, 77 88. Available from: https://doi.org/10.1016/j.envexpbot.2016.07.004. Mallory, A.C., Vaucheret, H., 2006. Functions of microRNAs and related small RNAs in plants. Nat. Gene 38, 31 36. Okupnik, A., Pflugmacher, S., 2016. Oxidative stress response of the aquatic macrophyte Hydrilla verticillata exposed to TiO2 nanoparticles. Environ. Toxicol. Chem. 35, 2859 2866. Available from: https://doi.org/ 10.1002/etc.3469. Prasad, T., Sudhakar, P., Sreenivasulu, Y., Latha, P., Munaswamy, V., Reddy, K.R., et al., 2012. Effect of nanoscale zinc oxide particles on the germination, growth and yield of peanut. J. Plant. Nutr. 35, 905 927. Available from: https://doi.org/10.1080/01904167.2012.663443. Priester, J.H., Ge, Y., Mielke, R.E., Horst, A.M., Moritz, S.C., Espinosa, K., et al., 2012. Soybean susceptibility to manufactured nanomaterials with evidence for food quality and soil fertility interruption. Proc. Natl. Acad. Sci. U.S.A. 109, E2451 E2456. Available from: https://doi.org/10.1073/pnas.1205431109. Ramesh, M., Palanisamy, K., Babu, K., Sharma, N.K., 2014. Effects of bulk & nano-titanium dioxide and zinc oxide on physio-morphological changes in Triticum aestivum Linn. J. Global Biosci. 3, 415 422. Shah, A.N., Tanveer, M., Hussain, S., Yang, G., 2016. Beryllium in the environment: whether fatal for plant growth? Rev. Environ. Sci. Bio/Tech. 15 (4), 549 561. Shukla, L.I., Chinnusamy, V., Sunkar, R., 2008. The role of microRNAs and other endogenous small RNAs in plant stress response. Biochim. Biophys. Acta 1779, 743 748. Zhang, B., Pan, X., Cobb, G.P., Anderson, T.A., 2006a. Plant microRNA: a small regulatory molecule with big impact. Dev. Biol. 289, 3 16. Zhang, H.M., Quan, X., Chen, S., Zhao, H.M., 2006b. Fabrication and characterization of silica/titania nanotubes composite membrane with photocatalytic capability. Environ. Sci. Technol. 40, 6104 6109. Zhao, L., Sun, Y., Hernandez-Viezcas, J.A., Servin, A.D., Hong, J., Niu, G., et al., 2013. Influence of CeO2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: a life cycle study. J. Agric. Food. Chem. 61, 11945 11951.

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C H A P T E R

25 The role of aquaporins during plant abiotic stress responses Aditya Banerjee and Aryadeep Roychoudhury Department of Biotechnology, St. Xavier’s College (Autonomous), Kolkata, India

25.1 Introduction Adverse environmental conditions involving both edaphic and atmospheric abnormalities lead to large-scale crop losses throughout the world (Banerjee and Roychoudhury, 2017a). The dearth of fresh water in the global context is mostly responsible for serious ecological and agronomical crisis. Large stretches of agricultural lands now stand barren due to increase in saline or heavy metal contents. Atmospheric stresses, such as extremes of temperatures, also pose severe threats to agricultural expansion pursuits (Banerjee and Roychoudhury, 2018a,b). Plants are diverse organisms, which have developed multiple evolutionary strategies to adapt to such suboptimal conditions. The entire systemic machinery undergoes significant alterations at transcriptomic, proteomic, metabolomic, and even epigenomic levels to tackle abiotic stresses (Banerjee and Roychoudhury, 2018c). It has been observed that the regulation of intra- and inter-transport of water among cells and tissues is vital for plants during any kind of stress. Thus a thorough understanding of the plant water relations and transport is necessary to identify potential molecular targets that might be modified to generate abiotic stress tolerance. The major transporters facilitating efficient exchange of water molecules and small, uncharged solutes are the group of membrane protein named “aquaporins” (AQPs) (Surbanovski and Grant, 2014). These transmembrane channel proteins mediate transport of the abovementioned molecules across the membrane. Hence, they are also referred to as “water channels” (Surbanovski and Grant, 2014). More than 30 genes (classified into multiple subfamilies) encode the AQPs (Maurel et al., 2015). These genes are induced by diverse physiological cues including abiotic stresses, such as salinity, drought, cold, and heavy-metal toxicity. The optimal flow of water from source to sink is regulated by AQPs. This aids in the movement of water to those tissues where it is most critically required under emergency conditions (Aroca et al., 2012). The temporal control of upregulation of specific AQP

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00028-X

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isoforms crucially dictates plant adaptation to stress situations. The expressions of AQPs vary with the plant cultivar and even stress conditions (Surbanovski and Grant, 2014). In view of their functions in mediating water transport, AQPs also promote dynamic alterations in the hydraulic conductivities in leaf, stem, and root tissues. This acts as a checkpoint for water usage under normal and especially suboptimal conditions (Sade and Moshelion, 2017). The vascular AQPs mediate leaf hydraulic conductivity, water-use efficiency and determine the rate of growth, reproduction, and production (Sade and Moshelion, 2017). This chapter illustrates the diverse roles and participation of AQPs under different abiotic stresses. The discussion would better aid in understanding AQP dynamics in the context of plant abiotic stress physiology.

25.2 Brief history of aquaporins Initially, since the discovery of the lipid bilayer in the 1920s, water flow within tissues was thought to be mediated by simple diffusion. However, diffusion across lipid membrane is physiologically very slow and cannot support the rapid transport of significant volumes of water. Hence, the idea of specialized pores was proposed (Maurel et al., 1997). Identification of the abundant transmembrane integral protein, CHIP28 in human erythrocytes in the late 1980s raised the idea regarding the proteinaceous nature of the specialized membrane pores in plants (Macey and Farmer, 1970; Denker et al., 1988). The first AQP to be identified in plants was NODULIN-26 (NOD26) from Glycine max (Fortin et al., 1987). The functional significance of a plant AQP was deciphered by expressing Arabidopsis TONOPLAST INTRINSIC PROTEIN 1;1 (TIP1;1) in the oocytes of Xenopus laevis (Maurel et al., 1993). AQPs are the members of a superfamily of membrane proteins, MAJOR INTRINSIC PROTEIN (MIP), which have been detected in all organisms except thermophilic archaea and intracellular bacteria (Abascal et al., 2014). AQPs are also involved in the transport of solutes, such as glycerol, urea, carbon monoxide, ammonia, metalloids, and even reactive oxygen species (ROS) (Maurel et al., 2015) (Fig. 25.1). Plants do not have a specialized circulatory system and rely on AQPs for efficient circulation of solvents and selected solutes. Hence, these proteins have tremendous impacts during abiotic stress responses in plants. Table 25.1 represents the number of AQPs that have been identified in different plant species.

25.3 Aquaporins: functional and structural significance in plants AQPs can be classified into three major subclasses based on their substrate specificity and sequence conservation. These are (1) AQPs, which mediate the transport of water along with dissolved ions; (2) aquaglyceroporins (GLAs), which are involved in water and glycerol transport; and (3) glycerol-facilitator AQPs (GLPs), which transport water and neutral molecules (Karkouri et al., 2005). Plants lack the presence of GLP orthologs. However, a large diversity of AQPs has been detected in these organisms in comparison to mammals, which contain only 13 AQP isoforms strictly localized in the secretory glands and fluid-containing organs (Nielsen et al., 1997). The AQP diversity in plants is so pronounced that these proteins can be classified into seven subfamilies based on their localization and sequence

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FIGURE 25.1 The structural motifs in aquaporins. This group of transporters contains six alpha helical transmembrane helices (TM1 TM6) along with five interhelical loops (LA LE) for facilitating limited structural mobility. Two conserved Asp-Pro-Ala (NPA) motifs are detected. The N-terminal domain contains Ala-Glu-Phe within an AEFXXT motif. Source: Extracted from Afzal, Z., Howton, T.C., Sun, Y., Mukhtar, M.S., 2016. The roles of aquaporins in plant stress responses. J. Dev. Biol. 4, 9.

TABLE 25.1

Number of aquaporins (AQPs) identified across plant species.

Species

Number of AQPs

References

Zea mays

31

Chaumont et al. (2001)

Oryza sativa

33

Sakurai et al. (2005)

Capsella rubella

34

Sonah et al. (2017)

Citrus sinensis

34

Martins et al. (2015)

Arabidopsis thaliana

35

Johanson et al. (2001)

Capsella grandiflora

37

Sonah et al. (2017)

Eutrema salsugineum

37

Arabidopsis lyrata

38

Sorghum bicolor

41

Reddy et al. (2015)

Solanum lycopersicum

47

Reuscher et al. (2013)

Musa sp.

50

Shekhawat and Ganapathi (2013)

Populus trichocarpa

55

Gupta and Sankararamakrishnan (2009)

Brassica oleracea

57

Sonah et al. (2017)

Brassica rapa

59

Kayum et al. (2017)

Glycine max

66

Ali et al. (2013)

Gossypium hirsutum

71

Park et al. (2012)

Brassica napus

120

Sonah et al. (2017)

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FIGURE 25.2 AQPs are localized in various subcellular organelles. The plasma membrane contains PIPs, XIPs, and NIPs. The ER harbors NIPs and SIPs. As their name suggests, TIPs are detected on the vacuolar membrane, tonoplasts. AQPs, Aquaporins; ER, endoplasmic reticulum; NIPs, NODULIN-26 LIKE INTRINSIC PROTEINS; PIPs, PLASMA MEMBRANE INTRINSIC PROTEINS; SIPs, SMALL BASIC INTRINSIC PROTEINS; TIPs, TONOPLAST INTRINSIC PROTEINS; XIPs, UNCATEGORIZED X INTRINSIC PROTEINS. Source: Extracted from Afzal, Z., Howton, T.C., Sun, Y., Mukhtar, M.S., 2016. The roles of aquaporins in plant stress responses. J. Dev. Biol. 4, 9.

pattern: plasma-membrane intrinsic proteins (PIPs), TIPs, NOD26-like intrinsic proteins (NIPs), small, basic intrinsic proteins (SIPs), the GlpF-like intrinsic proteins, hybrid intrinsic protein, and the uncategorized X intrinsic protein (XIP) (Forrest and Bhave, 2007) (Fig. 25.2). The subfamilies can be further divided into multiple isoforms depending on the localization and functional properties (Forrest and Bhave, 2007). PIPs and TIPs are localized in the cell membrane and vacuolar tonoplast, respectively. Some of these transporters have been found in the inner envelope and thylakoids in Arabidopsis (Maurel et al., 2015). The solvent transport in the endoplasmic reticulum (ER) is mediated by the SIPs and some NIPs (Maurel et al., 2015). Interestingly, NIPs have the capability to transport water and some of the previously mentioned solutes between host plants and bacterial symbionts. The TIPs and NIPs are thus less permeable to water compared to PIPs and are mainly involved in the passage of organic microcompounds and minerals (Ma et al., 2008; Zangi and Filella, 2012; Zhao et al., 2010). Permeability to water, metalloids, and ROS is mediated by the multifunctional XIP transporters. Lopez et al. (2012) reported the differential expression pattern of XIP2;1 in the leaves and stems of Populus plants treated with salicylic acid or exposed to drought or wounding. Apart from the typical water transport, proteins belonging to the MIP family might be permeable to unconventional substrates, such as arsenite, antimony, boron, silicon, ammonia, carbon dioxide, formamide, urea, hydrogen peroxide (H2O2), and lactic acid. In spite of such functional variability, the MIPs can contain six transmembrane α-helices (TM-1 to TM-6) along with five intermediate loops (LA LE), conserved Ala-Glu-Phe residues within an AEFXXT motif in the N-terminal domain and conserved Asn (N)-Pro (P)-Ala (A) (NPA) residues within two NPA motifs (NPA boxes) (Afzal et al., 2016). The substrate selectivity and specificity is dictated by the NPA boxes and residues in the aromatic/Arg stretch. The NPA box chiefly contributes to water transport (Forrest and Bhave, 2007). The PIPs and TIPs participate in abiotic stress responses during salinity, drought, and cold (Afzal et al., 2016).

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25.4 Water dynamics and aquaporins Plants are autotrophic organisms, which can photosynthesize and prepare their own food (photosynthet). In this process, photons from aerial sunlight and soil water containing dissolved mineral nutrients are required (Banerjee and Roychoudhury, 2016a). Thus an optimized circulation of water throughout the system is quintessential for stabilizing the crucial physiological activities in plants. Plant water relations are known to have tremendous impact during fluctuating edaphic and atmospheric conditions (Banerjee and Roychoudhury, 2017b). Thus optimum activities of AQPs are necessary for the plant to maintain a soil plant atmosphere continuum. It is also interesting to know that only a very small percent (0.5%) of the total water absorbed is metabolized by plants. The remaining 99.5% is released during transpiration in order to equilibrate internal temperature of the plants (Freeman, 2007). Several kilograms of water are absorbed by plant roots to fix 1 kg of carbon during photosynthesis (Freeman, 2007). The absorbed water is channelized to either of the three routes: (1) apoplastic pathway along the cell wall, (2) symplastic pathway along the cytoplasm of adjacent cells through the plasmodesmata, and (3) transcellular pathway via the plasma membrane (Tyerman et al., 2002). Large proportions of water to be transported to long distances are directed to the apoplastic pathway that facilitates solvent passage across the vascular bundles without any hindrance from the cell membranes (Kaldenhoff et al., 2008). High water potential (ΔΨ) promotes water transport via capillary action across the vascular bundles (Tyerman et al., 2002; Kaldenhoff et al., 2008). AQPs are usually involved in short-distance transport required to maintain cellular turgor and physiological metabolism. These transporters regulate osmoregulation, leaf and root hydraulic conductivities, cell elongation, and transpiration (Wallace et al., 2006; Siefritz et al., 2002; Sade et al., 2010; Hukin et al., 2002). AQPs regulate effective water circulation in order to equilibrate the cellular osmotic potential during suboptimal environmental conditions such as drought, salinity, extremes of temperature, heavy-metal toxicity (abiotic stress), and even pathogen infections (biotic stress) (Sade et al., 2010). Exposure to any kind of abiotic stress induces metabolic reprogramming of the cellular machinery in order to restrict water loss by promoting stomatal closure and other water-conservation strategies. Thus due to an overall reduction in the absorption of CO2, plant biomass production is reduced under abiotic stresses (Park and Campbell, 2015). The potential roles of AQPs in the complicated signaling array of abiotic stress responses are largely unknown. The mechanistic routes of AQPs in promoting abiotic stress tolerance are under investigation. A number of transcriptomic experiments carried out at the varietal levels and under different environmental cues portray differential expression of AQP genes in a tissue- and stressdependent manner (Afzal et al., 2016).

25.5 Roles of aquaporins in abiotic stresses Due to high diversity of AQPs in plants, the signalosome regulated by AQPs during abiotic stresses is yet to be unraveled. However, several reverse genetics approaches have been adopted to understand the integral and complex expression pattern of these proteins

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under myriad environmental conditions. This section presents a comprehensive discussion on the roles of AQPs reported in plants exposed to environmental stress.

25.5.1 Aquaporins in drought/desiccation stress AQPs, such as PIPs and TIPs, are largely responsible for water uptake and transcellular solvent flow in the roots (Boursiac et al., 2008). AQP homologs are differentially expressed during drought stress. A drought-responsive AQP, PIP2;3 was detected in Arabidopsis plants exposed to desiccation stress (Yamaguchi-Shinozaki et al., 1992). Most PIP and some TIP genes exhibited elevated expression in Arabidopsis plants subjected to drought. However, the NIP genes were expressed at very low levels (Alexandersson et al., 2005). Interestingly, only the AtPIP1;4 and AtPIP2;5 genes were upregulated in the leaves of the stressed plants. AtPIP2;6 and AtSIP1;1 exhibited constitutive expression under both control and stress conditions (Alexandersson et al., 2005). Interestingly, heat stress also induced the expression of AtPIP2;5 gene (Rizhsky et al., 2004). It has been documented that a large fraction of PIP genes are suppressed, while some are activated during drought stress in Arabidopsis (Alexandersson et al., 2010). A majority of the PIP genes were reported to be downregulated during desiccation in the roots of tobacco, peach fruits, and in the twigs and roots of olive plants (Mahdieh et al., 2008; Secchi et al., 2007). Species-dependent contrasting variability of expression has also been observed in the case of AQP homologs. In Vitis vinifera the expression of PIP1;1 in the roots was induced during drought only in an anisohydric (risk-taking) cultivar but not in the isohydric counterpart (Vandeleur et al., 2009). Park et al. (2012) reported opposite expression patterns of highly homologous genes, PIP1;3 and PIP1;1 in the leaves and roots of Gossypium hirsutum under control and drought conditions. Thus in spite of sequence homology, these genes exhibit contrasting expression under desiccation. The polyethylene glycol (PEG) mediated drought stress in rice showed the induction of OsPIP1;1 and OsPIP1;2, though the expression of OsPIP1;3, remained unchanged (Guo et al., 2006). Sonah et al. (2017) analyzed the RNA-seq data of AQPs in canola plants. They reported high level of conservation in the distribution and spacing between the NPA domains and selectivity filters. High expression of TIP3s was identified in the developing seeds due to its potential role in regulating desiccation (Sonah et al., 2017). The expression of 70% of the AQP genes was observed to be dose-independent, which indicated their participation in stress-alleviation responses (Sonah et al., 2017). The PIP1 gene in the leguminous plant, Galega orientalis, was found to be associated with drought tolerance (Li et al., 2015). GoPEP1 exhibited elevated expression pattern in the roots under both NaCl- and PEGmediated stress. Interestingly, overexpression of this gene in Arabidopsis yielded droughtsensitive, yet salt-tolerant transgenics (Li et al., 2015). The activities of PIP1;1 and PIP2;1 in Fragaria vesca were found to be affected by diurnal rhythms under drought stress, as their expression corresponded to lowering of substrate moisture contents (Surbanovski et al., 2013). The variable expression of TIP1;2, TIP2;3, and NIP2;1 was observed in Zea mays plants inoculated with arbuscular mycorrhizal fungi and exposed to drought stress (Barzana et al., 2014). Yu et al. (2005) overexpressed PIP1 gene from Brassica napus and reported increased drought tolerance in the transgenic tobacco plants. Overexpression of AQP7 from Triticum

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aestivum also developed drought tolerance in the genetically engineered tobacco plants due to the elevated capacity to retain water (Zhou et al., 2012). The tolerance to drought was also observed in the transgenic Arabidopsis plants constitutively expressing the PIP1 gene from Vicia faba. The transgenics exhibited prompt stomatal closure and transpirationmediated water loss during stress (Cui et al., 2008). Overexpression of PIP1;1 and PIP1;2 genes from banana in Arabidopsis conferred elevated drought tolerance (Xu et al., 2014). Transgenic tomato plants overexpressing the endogenous SlTIP2;2 gene were reported to be drought tolerant (Sade et al., 2009). Dissection of the root transcriptome of chickpea plants exposed to drought revealed a complex integration of PIPs, TIPs, and NIPs (Molina et al., 2008). Reduced root hydraulic conductivity was observed in plants with silenced PIP genes (Martre et al., 2002). Water passage via the protoplasm drastically reduced in the Arabidopsis knockout mutants of AtPIP1;2 and AtPIP2;2 (Javot et al., 2003). Almost 30-fold decrease in the root hydraulic pressure was observed in Arabidopsis plants with silenced AtPIP1 and AtPIP2 genes (Afzal et al., 2016). Even under control conditions, the knockout mutants of Physcomitrella patens of PpPIP2;1 and PpPIP2;2 showed wilted growth (Lienard et al., 2008). Gu et al. (2017) demonstrated an interesting DREB1B AQP correlation in transgenic F. vesca (strawberry) plants overexpressing RdreB1Bl gene. It was observed that RdreB1Bl activated the endogenous PIP2;1 like 1 promoter. Low rates of electrolyte leakage, malondialdehyde (MDA) content and increased drought tolerance, relative water content, and peroxidase (POX) and superoxide dismutase (SOD) activities could be observed in the transgenic plants in comparison to the control sets (Gu et al., 2017). This research highlights the DREB AQP interaction in mediating drought tolerance in strawberry plants. AQPs thus play crucial roles in water circulation across cells and tissues in the plant system. The transgenic and reverse genetics studies mentioned earlier clearly illustrate the immense roles of AQP genes in drought and desiccation stress responses. Thus these genes should be further characterized in order to identify the complex signaling networks involving them. Resurrection plants are potential model organisms for studying and screening desiccationtolerant genes. TIP3;1 was detected in the small vacuoles of the leaves of resurrection grass, Eragrostis nindensis. The transporter mobilized water and dissolved solutes from the vacuoles during drought (Willigen et al., 2004). Smith-Espinoza et al. (2003) reported the upregulation of some PIPs in Craterostigma plantagineum exposed to drought stress. Transgenic Arabidopsis plants overexpressing the endogenous gene, FaPIP2;1 from the perennial grass, Festuca arundinacea were tolerant to desiccation and leaf dehydration (Zhuang et al., 2015). AlmeidaRodriguez et al. (2010) reported a direct correlation between PIP genes and stomatal conductance in Populus balsamifera and Populus simonii X P. balsamifera. Researches on resurrection plants and drought-tolerant plants are relevant to agricultural pursuits since these investigations unfold unknown gene that can be introduced in the sensitive plant species. Due to direct correlation with transpiration and photosynthesis, CO2 conductivity is also reportedly regulated by PIPs. Thus under desiccating conditions, PIPs control CO2 conductivity and in turn affect the photosynthetic capacity. Transport of CO2 in the mesophyll tissues of Nicotiana tabacum is facilitated by NtAQP1 (Flexas et al., 2006). The heterotetramer formed by the association of MIPB (PIP1) and PIP2 in Mesembryanthemum crystallinum stimulated stomatal and mesophyll conductance and the diffusion of CO2. Thus cooverexpression of these genes can be beneficial as the transgenics might have improved water mobilization

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25. The role of aquaporins during plant abiotic stress responses

as well as CO2 conductivity and photosynthetic yield (Flexas et al., 2012). Rice plants overexpressing PIP2;1 from Hordeum vulgare exhibited increased CO2 conductance and assimilation. However, the plants were hypersensitive to salt stress (Hanba et al., 2004). Overexpression of the endogenous TIP2;2 gene in tomato resulted in transgenics with improved CO2 absorption and nutrient balance under stress (Sade et al., 2009). Tsuchihira et al. (2010) observed decreased rate of CO2 assimilation in the Eucalyptus plants having the expression of PIP1 and PIP2 genes cosuppressed by the presence of RsPIP1;1 from Raphanus sativus.

25.5.2 Aquaporins in salinity stress Apart from drought, soil salinity is the most widespread kind of environmental challenge to agricultural expansions. The toxic salt concentrations drastically reduced plant growth and viability. The plant yield is suppressed, and the cellular osmotic balance is disorganized (Banerjee and Roychoudhury, 2016a, 2017b). This type of physiological stress deteriorates root hydraulic conductivity (Banerjee and Roychoudhury, 2015, 2016b). Arabidopsis plants exposed to salt stress exhibited 60% 75% decrease in the expression of PIPs and TIPs (Shekhawat and Ganapathi, 2013). The tissue-specific expression of PIP2;1 was observed in salt-stressed H. vulgare plants. The PIP2;1 expression was low in the roots but high in the shoots of the stressed plants. Interestingly, the transgenic barley lines overexpressing this gene were hypersensitive to salt stress (Katsuhara et al., 2002, 2003). The exposure to salt stress led to the downregulation of several PIP genes in the roots, and one TIP gene in the leaves of M. crystallinum plants (Kirch et al., 2000). The universal stress hormone, abscisic acid (ABA) was found to downregulate PIP1 and PIP2, while PIP1;1, PIP1;5, and PIP2;4 were transiently induced in maize plants exposed to salinity (Zhu et al., 2005). Pang et al. (2010) reported that TIP5;1 in Arabidopsis was also responsible for the vacuolar sequestration of borate. Overexpression of this gene in Arabidopsis developed borate-tolerant transgenics (Pang et al., 2010). The tolerance to salt and drought was observed in transgenic Arabidopsis lines overexpressing the TIP1 gene from Panax ginseng (Peng et al., 2007). The redistribution of AQPs during salt stress has also been observed in Arabidopsis. Endocytosis of PIPs or formation of membrane rafts during salt stress can be responsible for the relocalization of AQP during salt stress (Dhonukshe et al., 2007; Li et al., 2011a). The AtTIP1;1 (tagged with green fluorescent protein (GFP) was detected in the intracellular spherical structures. PIP2;1 (tagged with GFP) was also found to recycle from the cell membrane via continuous cycles of exocytosis and endocytosis during salinity (Luu et al., 2012). Feng et al. (2018) showed that the Arabidopsis loss-of-function mutants of TIP2;2 were less sensitive to NaCl, mannitol, and PEG-mediated abiotic stresses compared to the wildtype plants. The mutant lines exhibited enhanced germination rate, root growth along with reduced ion leakage and MDA contents. The expression of crucial salt-responsive genes, such as salt overly sensitive 1 (SOS1), SOS2, and SOS3 and dehydration-responsive element binding 1A (DREB1A) were modulated in the mutated lines (Feng et al., 2018). Kong et al. (2017) reported that most of the AQPs in Beta vulgaris were responsive to abiotic stresses such as salinity and heat. Salt treatment of the model forage grass, F. arundinacea reduced the transcript level of PIP1;2 in the salt-tolerant variety (Pawlowicz et al., 2017).

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Chang et al. (2016) observed the ABA-independent upregulation of AQP1 gene (from Sesuvium portulacastrum) overexpressed in transgenic tobacco plants. This AQP1 gene was highly homologous to PIP genes and was highly induced in the leaves, stems, and roots during salt stress. However, the expression of this gene was hindered by exogenous treatment of ABA (Chang et al., 2016). The transgenic tobacco lines exhibited enhanced salt tolerance along with increased activities of SOD, POX, and catalase (CAT). The overall antioxidant machinery was therefore reprogrammed (Chang et al., 2016). Wang et al. (2015a) cloned the PIP2;1 gene from salt-tolerant apple rootstock Malus zumi Mats into Arabidopsis plants. MzPIP2;1 was found to be localized in the epidermal and vascular cells of roots, parenchyma cells around vessels through stems and the vascular tissues of leaves (Wang et al., 2015a). The transgenic Arabidopsis plants were tolerant to slight salt and drought stresses. However, the plants exhibited susceptibility to moderately high salinity (Wang et al., 2015a). Dehydration, salinity, and cold stresses induced the expression of the PIP2;1 gene in the leaves of Glycine soja plants. However, this gene was found to be downregulated in the roots in response to these abiotic stresses (Wang et al., 2015b). The Arabidopsis plants overexpressing the PIP2;1 gene (from G. soja) exhibited normal growth under control conditions. However, the level of their tolerance to multiple stresses such as salt and desiccation was reduced. Further observations clarified the negative impacts of GsPIP2;1 in the regulation of plant water potential (Wang et al., 2015b). The roles of NIPs in regulating salinity-induced responses are less known. Transgenic Arabidopsis plants overexpressing TaNIP from T. aestivum exhibited tolerance to salt stress. Exogenous application of ABA also upregulated the expression of TaNIP, suggesting the involvement of this stress phytohormone in NIP-mediated salt-tolerant responses (Gao et al., 2010). Zhang et al. (2017) overexpressed the GmSIP1;3 gene from G. max in tobacco plants. The transgenic lines showed retarded growth rate and significantly enhanced tolerance to H2O2-induced oxidative stress. The subcellular localization and colocalization studies confirmed the presence of GmSIP1;3 in the ER membrane. Interestingly, the indole acetic acid content was found to be elevated, and the ABA level was reduced in the transgenic plants (Zhang et al., 2017).

25.5.3 Aquaporins in low temperature stress Low temperature or cold stress is a significant kind of environmental stress, which interferes with cell membrane fluidity, cellular metabolism and hence negatively affects plant development and reproduction (Banerjee et al., 2017). The participation of AQPs in ameliorating cold susceptibility has been reported in some plant species. Cold stress affects the hydraulic conductivity of roots. AQPs such as PIPs are known to equilibrate such unwanted alteration of the root hydraulic conductivity and maintain the homeostasis of the systemic metabolome. Differential expression of PIPs has often been linked with recovery from cold stress (Afzal et al., 2016). Hence, the modulation of the genes encoding these transporters has been performed to verify the generation of cold-tolerant phenotype. Overexpression of the endogenous PIP1;2 in banana resulted in cold and drought tolerance in the transgenics (Shekhawat and Ganapathi, 2013). Generation of similar traits of cold and drought tolerance was also visible in the transgenic tobacco plants overexpressing AQP7 gene from T. aestivum (Zhou et al., 2012; Huang et al., 2014).

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The previous paragraph discusses the instances where cotolerance to both low temperature and drought stresses has been observed. However, the complexity of the AQP-mediated regulatory network does not allow such uniformity. Homologous overexpression of PIP1;4 and PIP2;5 in Arabidopsis promoted tolerance to cold stress. However, these genetically modified plants exhibited rapid dehydration under drought and hence could not tolerate this stress condition (Ahamed et al., 2012). Exposure to cold stress in rice plants resulted in increased root hydraulic conductivity and induction of OsPIP2;5 expression (Ahamed et al., 2012). The expression of TIP genes, such as OsTIP1;1 and OsTIP2;2, were suppressed and that of OsPIP1;3 was significantly induced in rice subjected to chilling stress (Sakurai et al., 2005). Auler et al. (2017) reported that exposure of rice plants to low temperature of 13 C induced the expression of TIP41 gene. Specific localization of PIP2;3 in the cell membrane of maize leaves contributed to the differing levels of chilling sensitivity (Bilska-Kos et al., 2016). It was reported that responses to moderate chilling temperature of 15 C could be mediated by PIP2;3 and the thick-walled sieve tubes (found specifically in monocotyledonous plants) (Bilska-Kos et al., 2016). Zhuo et al. (2016) reported that overexpression of PIP2-7 from Medicago falcata in tobacco yielded tolerance toward multiple abiotic stresses such as chilling, freezing, and even nitrate reduction. MfPIP2-7 was found to mobilize the diffusion of H2O2 in yeast. The transcript levels of genes, such as early responsive to dehydration 10B (ERD10B), ERD10C, DREB1, and DREB2, were found in elevated amounts in the transgenic tobacco plants (Zhuo et al., 2016). The ERD genes encode late embryogenesis abundant proteins, which crucially regulate cellular homeostasis and maintain the osmotic balance (Banerjee and Roychoudhury, 2016a). The transgenic tobacco plants overexpressing MfPIP2-7 also showed elevated activity of nitrate reductase leading to altered profiles of free amino acids in comparison to the control plants (Zhuo et al., 2016). Interestingly, among other PIPs, only PIP2;5 and PIP2;6 were found to be induced during cold stress. Usually, these genes are expressed at a very low level under normal conditions. In spite of the fact that ABA acts as the universal stress hormone in plants, a complex integration of ABA-dependent and ABA-independent pathways is known to regulate AQP expression. The responses of each AQP gene to ABA treatment has been found to be variable, indicating toward the presence of ABA-dependent and ABA-independent signaling cascades involved in AQP expression (Li et al., 2015). Temporal variability of chilling stress differentially affected the expression of PIP genes in the cold-sensitive and cold-tolerant cultivars of maize. The tolerant variety exhibited responses that facilitated poststress recovery. These responses were not observed in the cold-susceptible maize cultivar (Aroca et al., 2005; Nogueira et al., 2003).

25.5.4 Aquaporins in trace element transport and heavy-metal toxicity The roles of NIPs in abiotic stress responses are less characterized. Limited literature is available on the roles of these AQP homologs in environmental adversities such as salinity, drought, and extreme temperature. Functional characterization of NIPs in mediating water transport is less documented. The transporters encoded by NIP genes mobilize the intercellular passage of nutrients along with water (Afzal et al., 2016). The growth of Arabidopsis nip5;1 knockout mutants was drastically inhibited under limited concentration of boron (B) (Takano et al., 2006). The essential micronutrient B is a

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trace element, which determines optimum growth, development, and reproduction of plants. Thus the deficiency of this trace element leads to critical edaphic stress on cultivated crop species. As a result, plants succumb to this type of nutrient deficiency causing significant global crop losses (Takano et al., 2006). The AtNIP5;1 has been reported to be involved in mediating B homeostasis in Arabidopsis. This inference could be drawn from the feedback inhibition of AtNIP5;1 gene in response to high supply of B (Li et al., 2011b). The ortholog of AtNIP5;1 in Z. mays was detected as ZmNIP3;1. This gene was also found to mediate the abnormal phenotype conferred by limited supply of B. Kato et al. (2009) reported that the activation tagging of NIP5;1 in Arabidopsis ensured proper root elongation during B-deficient conditions. The transport and distribution of B in the shoots and anthers of Arabidopsis are regulated by the NIP6;1 and NIP7;1 homologs, respectively (Tanaka et al., 2008). Hanaoka et al. (2014) reported the roles of AtNIP5;1 and AtNIP6;1 homolog, OsNIP3;1, to facilitate B transport in rice. B was imported at a higher rate in the yeast cells overexpressing OsNIP3;1 compared to the control cells (Hanaoka et al., 2014). Overexpression of OsNIP3;1 in the tobacco BY2 cells led to high accumulation of NIP3;1 transcripts in the roots of the transgenics exposed to high concentration of B. Further localization experiments confirmed the presence of this transporter in exodermal cells and steles in roots; in the cells of vascular bundles in leaf sheaths and in those of the pericycle around the leaf blade xylem (Hanaoka et al., 2014). The RNAi knockdown lines exhibited severe growth inhibition under B deficiency. Thus the roles of OsNIP3;1 are essential for plant survival and development (Hanaoka et al., 2014). Xu et al. (2015) identified AtNIP3;1 in Arabidopsis to mediate the uptake and systemic distribution of As under As(III) stress. Heterologous expression of the gene in yeast enabled the transformed cells to import As(III). The AtNIP3;1 was characterized as a passive and bidirectional As(III) transporter in Arabidopsis (Xu et al., 2015). The NIP transporters are also known to play roles in arsenic (As) and antimony (Sb) transport in crop plants (Azad et al., 2018). Investigations regarding the group-wise substrate-selectivity profiles in NIPs led to the identification of specific amino acid residues in the pore line, loop D, and termini. Transcript profiling revealed that the NIPs involved in As and Sb transport were highly expressed in the roots (Azad et al., 2018). The Arabidopsis loss-of-function mutants of NIP1;1 exhibited elevated tolerance toward Sb-mediated stress (Kamiya and Fujiwara, 2009). Chen et al. (2017) reported that OsNIP3;2 mediates arsenite [As(III)] import via the lateral roots in rice plants. The oocytes of X. laevis expressing OsNIP3;2 exhibited increased accumulation of As(III). Interestingly, low concentration of As (III) (5 μM) suppressed OsNIP3;2 expression, whereas higher concentrations of 20 and 100 μM significantly induced it (Chen et al., 2017). The localization studies showed that the transporter was expressed in the lateral roots and stele of the primary roots. The rice knockout mutants of OsNIP3;2 accumulated less amount of As(III) compared to the control plants (Chen et al., 2017). The authors inferred that OsNIP3;2 participated in As(III) import via the lateral roots; however, the role of this transporter in the accumulation of As in plant shoots is less characterized (Chen et al., 2017). The role of the aquaglyceroporin, AtNIP7;1, in As (III) uptake in Arabidopsis has been documented (Lindsay and Maathuis, 2016). The loss-offunction mutants of this gene reduced As levels in the xylem and phloem and promoted tolerance toward arsenate [As(V)] (Lindsay and Maathuis, 2016). In view of their ability to transport several metalloids, the NIPs are also referred to as physiologically essential

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metalloido-porins (Pommerrenig et al., 2015). The elevated level of tolerance was observed in Arabidopsis double knockout mutants of AtNIP1;1 and AtNIP3;1 (Bienert et al., 2008). Silicon (Si) is an important element with protective and ameliorative effects during multiple abiotic stresses (Yamaji et al., 2008). Quantitative trait loci mapping in a set of rice plant exhibiting defective Si uptake was used to identify OsNIP2;1 as a crucial Si transporter in rice (Ma et al., 2006). Studies by Yamaji et al. (2008) revealed the existence of NIP2;2 as a Si transporter in rice. A lactic acid transporter, AtNIP2;1, which is induced under anaerobic conditions was found to be associated with submergence stress in Arabidopsis plants (Choi and Roberts, 2007).

25.6 Conclusion and future perspectives Various experimental evidences as discussed throughout the chapter clearly indicate the diverse roles of AQPs in generating tolerance to multiple abiotic stresses (Fig. 25.3). Thus these transporters can be investigated as potential molecular targets, which can be genetically overexpressed to develop abiotic stress tolerance phenotypes in crop plant species distributed across the world. However, much of the information regarding the activity of AQPs is yet to be retrieved. This can be accredited to the complex integrated signaling cascades involved in mediating condition-specific responsiveness of AQPs. The physiological responses of AQPs can be more complicated in the transgenic plants overexpressing heterologous AQP genes from foreign plant species. This is because the heterologous AQP might exhibit unknown interactions with the cellular and molecular components of the host plant. Such observations have been reported in Arabidopsis plants overexpressing the PIP1 gene from V. faba. The transgenic lines were tolerant to drought due to efficient stomatal closure and low rate of water loss (Cui et al., 2008). Expression of PIP1;1 gene from R. sativus in Eucalyptus globulus plants resulted in complete silencing of the endogenous EgPIP1 and EgPIP2 genes (Tsuchihira et al., 2010). The stomatal density increased in the transgenic tobacco plants overexpressing the Arabidopsis PIP1b gene. However, the plants FIGURE 25.3 Different abiotic stress responses are mediated through different transporters belonging to the AQP family, in an integrated and cooperative pattern. XIPs are induced in drought in a salicylic acid-responsive pathway. However, drought, salinity, and cold stress are together regulated via PIPs and TIPs. The NIPs are involved in environmental stresses like nutrient starvation/ deficiency and heavy-metal toxicity. AQPs, Aquaporins; NIPs, NODULIN-26 LIKE INTRINSIC PROTEINS; PIPs, PLASMA MEMBRANE INTRINSIC PROTEINS; TIPs, TONOPLAST INTRINSIC PROTEINS; XIPs, uncategorized X intrinsic proteins.

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succumbed to drought stress due to excess loss of water (Aharon et al., 2003). Ayadi et al. (2011) reported enhanced osmotic stress tolerance in the transgenic lines of tobacco overexpressing the PIP1;1 gene from Triticum turgidum. The genetically modified plants exhibited increased leaf area and root length (Ayadi et al., 2011). Jang et al. (2007) showed that the entire stress response pattern gets affected along with the expression of other AQP genes in transgenic Arabidopsis plants overexpressing the PIP isoforms, CfPIP2;1 and CfPIP1;1 from Cucurbita ficifolia and Cucumis sativus, respectively. Several studies on interactomics have shown the possible physical interactions that could occur among different AQP homologs, thus opening a novel avenue for research (Zelazny et al., 2007; Chen et al., 2013; Li et al., 2013). The interactions of AQPs with other proteins involved in different signaling pathways have also been hypothesized and experimentally determined (Besserer et al., 2012; Hachez et al., 2014a,b; Lee et al., 2009; Masalkar et al., 2010; Wu et al., 2013). The chapter highlights the various influences of AQPs on plant abiotic stresses such as salinity, drought, desiccation, temperature extremes, nutrient starvation, and heavy-metal toxicity. The complicated and diverse responses by AQPs demand further experimental validations at genomic, transcriptomic, and proteomic levels. Epigenomic studies involving the identification of various epigenetic mechanisms regulating AQP expression under various stimuli can provide novel data. The various signaling pathways activating AQP expression need to be mapped and properly defined. Only then the mechanistic participation of AQPs in plant abiotic stresses could be better and more precisely understood.

Acknowledgments The financial support from the Council of Scientific and Industrial Research (CSIR), Government of India through the research grant [38(1387)/14/EMR-II] to Dr. Aryadeep Roychoudhury is gratefully acknowledged. The authors thank the University Grants Commission, Government of India for providing Junior Research Fellowship to Mr. Aditya Banerjee.

References Abascal, F., Irisarri, I., Zardoya, R., 2014. Diversity and evolution of membrane intrinsic proteins. Biochim. Biophys. Acta Gen. Subj. 1840, 1468 1481. Afzal, Z., Howton, T.C., Sun, Y., Mukhtar, M.S., 2016. The roles of aquaporins in plant stress responses. J. Dev. Biol. 4, 9. Ahamed, A., Murai-Hatano, M., Ishikawa-Sakurai, J., Hayashi, H., Kawamura, Y., Uemura, M., 2012. Cold stress-induced acclimation in rice is mediated by root-specific aquaporins. Plant Cell Physiol. 53, 1445 1456. Aharon, R., Shahak, Y., Wininger, S., Bendov, R., Kapulnik, Y., Galili, G., 2003. Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15, 439 447. Alexandersson, E., Fraysse, L., Sjovall-Larsen, S., Gustavsson, S., Fellert, M., Karlsson, M., et al., 2005. Whole gene family expression and drought stress regulation of aquaporins. Plant Mol. Biol. 59, 469 484. Alexandersson, E., Danielson, J.A., Rade, J., Moparthi, V.K., Fontes, M., Kjellbom, P., et al., 2010. Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress. Plant J. 61, 650 660. Ali, Z., Wang, C.B., Xu, L., Yi, J.X., Xu, Z.L., Liu, X.Q., et al., 2013. Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). PLoS One 8, e56312. Almeida-Rodriguez, A.M., Cooke, J.E., Yeh, F., Zwiazek, J.J., 2010. Functional characterization of drought responsive aquaporins in Populus balsamifera and Populus simonii X balsamifera clones with different drought resistance strategies. Physiol. Plant. 140, 321 333.

Plant Life under Changing Environment

656

25. The role of aquaporins during plant abiotic stress responses

Aroca, R., Amodeo, G., Fernandez-Illescas, S., Herman, E.M., Chaumont, F., Chrispeels, M.J., 2005. The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol. 137, 341 353. Aroca, R., Porcel, R., Manuel Ruiz-Lozano, J., 2012. Regulation of root water uptake under abiotic stress conditions. J. Exp. Bot. 63, 43 57. Auler, P.A., Benitez, L.C., do Amaral, M.N., Vighi, I.L., Rodrigues, G.S., da Maia, L.C., et al., 2017. Selection of candidate reference genes and validation for real time PCR studies in rice plants exposed to low temperatures. Genet. Mol. Res. Available from: https://doi.org/10.4238/gmr16029695. Ayadi, M., Cavez, D., Miled, N., Chaumont, F.O., Masmoudi, K., 2011. Identification and characterization of two plasma membrane aquaporins in durum wheat (Triticum turgidum L. Subsp. Durum) and their role in abiotic stress tolerance. Plant. Physiol. Biochem. 49, 1029 1039. Azad, A.K., Ahmed, J., Alum, M.A., Hasan, M.M., Ishikawa, T., Sawa, Y., 2018. Prediction of arsenic and antimony transporter major intrinsic proteins from the genomes of crop plants. Int. J. Biol. Macromol. 107, 2630 2642. Banerjee, A., Roychoudhury, A., 2015. WRKY proteins: signaling and regulation of expression during abiotic stress responses. Sci. World J. 2015, 807560. Banerjee, A., Roychoudhury, A., 2016a. Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul. 79, 1 17. Banerjee, A., Roychoudhury, A., 2016b. Plant responses to light stress: oxidative damages, photoprotection and role of phytohormones. In: Ahammed, G.J., Yu, J.-Q. (Eds.), Plant Hormones Under Challenging Environmental Factors. Springer, Netherlands, pp. 181 213. Banerjee, A., Roychoudhury, A., 2017a. Epigenetic regulation during salinity and drought stress in plants: histone modifications and DNA methylation. Plant Gene 11, 199 204. Banerjee, A., Roychoudhury, A., 2017b. Abscisic-acid-dependent basic leucine zipper (bZIP) transcription factors in plant abiotic stress. Protoplasma 254, 3 16. Banerjee, A., Roychoudhury, A., 2018a. Effect of salinity stress on growth and physiology of medicinal plants. In: Ghorbanpour, M., et al., (Eds.), Medicinal Plants and Environmental Challenges. Springer International Publishing AG, Cham, Switzerland, pp. 177 188. Banerjee, A., Roychoudhury, A., 2018b. Regulation of photosynthesis under salinity and drought stress. In: Singh, V.P., Singh, S., Singh, R., Prasad, S.M. (Eds.), Environment and Photosynthesis: A Future Prospect. Studium Press (India) Pvt. Ltd., pp. 134 144. Banerjee, A., Roychoudhury, A., 2018c. The gymnastics of epigenomics in rice. Plant Cell Rep. 37, 25 49. Banerjee, A., Wani, S.H., Roychoudhury, A., 2017. Epigenetic control of plant cold responses. Front. Plant Sci. 8, 1643. Barzana, G., Aroca, R., Bienert, G.P., Chaumont, F.O., Ruiz-Lozano, J.M., 2014. New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol. Plant Microb. Interact. 27, 349 363. Besserer, A., Burnotte, E., Bienert, G.P., Chevalier, A.S., Errachid, A., Grefen, C., et al., 2012. Selective regulation of maize plasma membrane aquaporin trafficking and activity by the snare SYP121. Plant Cell 24, 3463 3481. Bienert, G.P., Thorsen, M., Schussler, M.D., Nilsson, H.R., Wagner, A., Tamas, M.J., et al., 2008. A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol. 6, 26. Bilska-Kos, A., Szczepanik, J., Sowinski, P., 2016. Cold induced changes in the water balance affect immunocytolocalization pattern of one of the aquaporins in the vascular system in the leaves of maize (Zea mays L.). J. Plant. Physiol. 205, 75 79. Boursiac, Y., Boudet, J., Postaire, O., Doan, T.L., Colette, T.R., Maurel, C., 2008. Stimulus induced downregulation of root water transport involves reactive oxygen species activated cell signalling and plasma membrane intrinsic protein internalization. Plant J. 56, 207 218. Chang, W., Liu, X., Zhu, J., Fan, W., Zhang, Z., 2016. An aquaporin gene from halophyte Sesuvium portulacastrum, SpAQP1, increases salt tolerance in transgenic tobacco. Plant Cell Rep. 35, 385 395. Chaumont, F.O., Barrieu, F.O., Wojcik, E., Chrispeels, M.J., Jung, R., 2001. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol. 125, 1206 1215.

Plant Life under Changing Environment

References

657

Chen, W., Yin, X., Wang, L., Tian, J., Yang, R., Liu, D., et al., 2013. Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1. Plant Mol. Biol. 83, 219 233. Chen, Y., Sun, S.K., Tang, Z., Liu, G., Moore, K.L., Maathuis, F.J.M., et al., 2017. The nodulin 26-like intrinsic membrane protein OsNIP3;2 is involved in arsenite uptake by lateral roots in rice. J. Exp. Bot. 68, 3007 3016. Choi, W.G., Roberts, D.M., 2007. Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J. Biol. Chem. 282, 24209 24218. Cui, X.H., Hao, F.S., Chen, H., Chen, J., Wang, X.C., 2008. Expression of the Vicia faba VfPIP1 gene in Arabidopsis thaliana plants improves their drought resistance. J. Plant. Res. 121, 207 214. Denker, B.M., Smith, B.L., Kuhajda, F.P., Agre, P., 1988. Identification, purification, and partial characterization of a novel MR 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 263, 15634 15642. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.D., et al., 2007. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17, 520 527. Feng, Z.J., Xu, S.C., Liu, N., Zhang, G.W., Hu, Q.Z., Xu, Z.S., et al., 2018. Identification of the AQP members involved in abiotic stress responses from Arabidopsis. Gene 646, 64 73. Flexas, J., Miquel, R.C., Hanson, D.T., Bota, J., Otto, B., Cifre, J., et al., 2006. Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J. 48, 427 439. Flexas, J., Barbour, M.M., Brendel, O., Cabrera, H.N.M., Carriquı´, M., Dı´az-Espejo, A., et al., 2012. Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci. 193, 70 84. Forrest, K.L., Bhave, M., 2007. Major intrinsic proteins (MIPs) in plants: a complex gene family with major impacts on plant phenotype. Funct. Integr. Genomics 7, 263 289. Fortin, M.G., Morrison, N.A., Verma, D.P.S., 1987. Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res. 15, 813 824. Freeman, S., 2007. Biological Science, third ed. Benjamin Cummins, NJ. Gao, Z., He, X., Zhao, B., Zhou, C., Liang, Y., Ge, R., et al., 2010. Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant Cell Physiol. 51, 767 775. Gu, X., Gao, Z., Yan, Y., Wang, X., Qiao, Y., Chen, Y., 2017. RdreB1Bl enhances drought tolerance by activating AQP-related genes in transgenic strawberry. Plant Physiol. Biochem. 119, 33 42. Guo, L., Wang, Z.Y., Lin, H., Cui, W.E., Chen, J., Liu, M., et al., 2006. Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res. 16, 277 286. Gupta, A.B., Sankararamakrishnan, R., 2009. Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol. 9, 134. Hachez, C., Laloux, T.E., Reinhardt, H., Cavez, D., Degand, H., Grefen, C., et al., 2014a. Arabidopsis snares syp61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability. Plant Cell 26, 3132 3147. Hachez, C., Veljanovski, V., Reinhardt, H., Guillaumot, D., Vanhee, C., Chaumont, F.O., et al., 2014b. The Arabidopsis abiotic stress-induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2;7 through protein-protein interactions and autophagic degradation. Plant Cell 26, 4974 4990. Hanaoka, H., Uraguchi, S., Takano, J., Tanaka, M., Fujiwara, T., 2014. OsNIP3;1, a rice boric acid channel, regulates boron distribution and is essential for growth under boron-deficient conditions. Plant J. 78, 890 902. Hanba, Y.T., Shibasaka, M., Hayashi, Y., Hayakawa, T., Kasamo, K., Terashima, I., et al., 2004. Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol. 45, 521 529. Huang, C., Zhou, S., Hu, W., Deng, X., Wei, S., Yang, G., et al., 2014. The wheat aquaporin gene TaAQP7 confers tolerance to cold stress in transgenic tobacco. Z. Naturforschung C 69, 142 148. Hukin, D., Doering-Saad, C., Thomas, C., Pritchard, J., 2002. Sensitivity of cell hydraulic conductivity to mercury is coincident with symplasmic isolation and expression of plasmalemma aquaporin genes in growing maize roots. Planta 215, 1047 1056. Jang, J.Y., Lee, S.H., Rhee, J.Y., Chung, G.C., Ahn, S.J., Kang, H., 2007. Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Mol. Biol. 64, 621 632.

Plant Life under Changing Environment

658

25. The role of aquaporins during plant abiotic stress responses

Javot, H.L.N., Lauvergeat, V., Santoni, V.R., Martin-Laurent, F., Guclu, J., Vinh, J.L., et al., 2003. Role of a single aquaporin isoform in root water uptake. Plant Cell 15, 509 522. Johanson, U., Karlsson, M., Johansson, I., Gustavsson, S., Sjovall, S., et al., 2001. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol. 126, 1358 1369. Kaldenhoff, R., Ribas-Carbo, M., Sans, J.F., Lovisolo, C., Heckwolf, M., Uehlein, N., 2008. Aquaporins and plant water balance. Plant Cell Environ. 31, 658 666. Kamiya, T., Fujiwara, T., 2009. Arabidopsis NIP1;1 transports antimonite and determines antimonite sensitivity. Plant Cell Physiol. 50, 1977 1981. Karkouri, K., Gueune, H., Delamarche, C., 2005. MIPDB: a relational database dedicated to MIP family proteins. Biol. Cell 97, 535 543. Kato, Y., Miwa, K., Takano, J., Wada, M., Fujiwara, T., 2009. Highly boron deficiency-tolerant plants generated by enhanced expression of NIP5;1, a boric acid channel. Plant Cell Physiol. 50, 58 66. Katsuhara, M., Akiyama, Y., Koshio, K., Shibasaka, M., Kasamo, K., 2002. Functional analysis of water channels in barley roots. Plant Cell Physiol. 43, 885 893. Katsuhara, M., Koshio, K., Shibasaka, M., Hayashi, Y., Hayakawa, T., Kasamo, K., 2003. Over-expression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell Physiol. 44, 1378 1383. Kayum, M.A., Park, J.-I., Nath, U.K., Biswas, M.K., Kim, H.-T., Nou, I.-S., 2017. Genome-wide expression profiling of aquaporin genes confer responses to abiotic and biotic stresses in Brassica rapa. BMC Plant Biol. 17, 23. Kirch, H.H., Vera-Estrella, R., Golldack, D., Quigley, F., Michalowski, C.B., Barkla, B.J., et al., 2000. Expression of water channel proteins in Mesembryanthemum crystallinum. Plant Physiol. 123, 111 124. Kong, W., Yang, S., Wang, Y., Bendahmane, M., Fu, X., 2017. Genome-wide identification and characterization of aquaporin gene family in Beta vulgaris. Peer J. 5, e3747. Lee, H.K., Cho, S.K., Son, O., Xu, Z., Hwang, I., Kim, W.T., 2009. Drought stress-induced RMA1H1, a ring membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21, 622 641. Li, X., Wang, X., Yang, Y., Li, R., He, Q., Fang, X., et al., 2011a. Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23, 3780 3797. Li, T., Choi, W.G., Wallace, I.S., Baudry, J., Roberts, D.M., 2011b. Arabidopsis thaliana NIP7;1: an anther-specific boric acid transporter of the aquaporin superfamily regulated by an unusual tyrosine in HELIX 2 of the transport pore. Biochemistry 50, 6633 6641. Li, D.D., Ruan, X.M., Zhang, J., Wu, Y.J., Wang, X.L., Li, X.B., 2013. Cotton plasma membrane intrinsic protein 2s (PIP2s) selectively interact to regulate their water channel activities and are required for fibre development. New Phytol. 199, 695 707. Li, J., Ban, L., Wen, H., Wang, Z., Dzyubenko, N., Chapurin, V., et al., 2015. An aquaporin protein is associated with drought stress tolerance. Biochem. Biophys. Res. Commun. 459, 208 213. Lienard, D., Durambur, G., Kiefer-Meyer, M.C., Nogue, F., Menu-Bouaouiche, L., Charlot, F., et al., 2008. Water transport by aquaporins in the extant plant Physcomitrella patens. Plant Physiol. 146, 1207 1218. Lindsay, E.R., Maathuis, F.J., 2016. Arabidopsis thaliana NIP7;1 is involved in tissue arsenic distribution and tolerance in response to arsenate. FEBS Lett. 590, 779 786. Lopez, D., Bronner, G.L., Brunel, N., Auguin, D., Bourgerie, S., Brignolas, F., et al., 2012. Insights into populus XIP aquaporins: evolutionary expansion, protein functionality, and environmental regulation. J. Exp. Bot. 63, 2217 2230. Luu, D.T., Martiniere, A., Sorieul, M., Runions, J., Maurel, C., 2012. Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J. 69, 894 905. Ma, J.F., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M., et al., 2006. A silicon transporter in rice. Nature 440, 688 691. Ma, J.F., Yamaji, N., Mitani, N., Xu, X.Y., Su, Y.H., McGrath, S.P., et al., 2008. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc. Natl. Acad. Sci. U.S.A. 105, 9931 9935.

Plant Life under Changing Environment

References

659

Macey, R.L., Farmer, R.E., 1970. Inhibition of water and solute permeability in human red cells. Biochim. Biophys. Acta Biomembr. 211, 104 106. Mahdieh, M., Mostajeran, A., Horie, T., Katsuhara, M., 2008. Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant Cell Physiol. 49, 801 813. Martins, C.D.P.S., Pedrosa, A.M., Du, D., Goncalves, L.P., Yu, Q., Gmitter Jr, F.G., et al., 2015. Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.). PLoS One 10, e0138786. Martre, P., Morillon, R.L., Barrieu, F.O., North, G.B., Nobel, P.S., Chrispeels, M.J., 2002. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol. 130, 2101 2110. Masalkar, P., Wallace, I.S., Hwang, J.H., Roberts, D.M., 2010. Interaction of cytosolic glutamine synthetase of soybean root nodules with the C-terminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J. Biol. Chem. 285, 23880 23888. Maurel, C., Reizer, J., Schroeder, J.I., Chrispeels, M.J., 1993. The vacuolar membrane protein gamma-tip creates water specific channels in xenopus oocytes. EMBO J. 12, 2241 2247. Maurel, C., Tacnet, F., Guclu, J., Guern, J., Ripoche, P., 1997. Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc. Natl. Acad. Sci. U.S.A. 94, 7103 7108. Maurel, C., Boursiac, Y., Luu, D.-T., Santoni, V., Shahzad, Z., Verdoucq, L., 2015. Aquaporins in plants. Physiol. Rev. 95, 1321 1358. Molina, C., Rotter, B.R., Horres, R., Udupa, S.M., Besser, B., Bellarmino, L., et al., 2008. Supersage: the drought stress-responsive transcriptome of chickpea roots. BMC Genomics 9, 553. Nielsen, S.R., King, L.S., Christensen, B.M.N., Agre, P., 1997. Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am. J. Physiol. Cell Physiol. 273, C1549 C1561. Nogueira, F.B.T., de Rosa, V.E., Menossi, M., Ulian, E.N.C., Arruda, P., 2003. RNA expression profiles and data mining of sugarcane response to low temperature. Plant Physiol. 132, 1811 1824. Pang, Y., Li, L., Ren, F., Lu, P., Wei, P., Cai, J., et al., 2010. Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J. Genet. Genomics 37, 389 397. Park, W.J., Campbell, B.T., 2015. Aquaporins as targets for stress tolerance in plants: genomic complexity and perspectives. Turk. J. Bot. 39, 879 886. Park, W., Scheffler, B.E., Bauer, P.J., Campbell, B.T., 2012. Genome-wide identification of differentially expressed genes under water deficit stress in upland cotton (Gossypium hirsutum L.). BMC Plant Biol. 12, 90. Pawlowicz, I., Rapacz, M., Perlikowski, D., Gondek, K., Kosmala, A., 2017. Abiotic stresses influence the transcript abundance of PIP and TIP aquaporins in Festuca species. J. Appl. Genet. 58, 421 435. Peng, Y., Lin, W., Cai, W., Arora, R., 2007. Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226, 729 740. Pommerrenig, B., Diehn, T.A., Bienert, G.P., 2015. Metalloido-porins: essentiality of nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci. 238, 212 227. Reddy, P.S., Rao, T.S.R.B., Sharma, K.K., Vadez, V., 2015. Genome-wide identification and characterization of the aquaporin gene family in Sorghum bicolor (L.). Plant Gene 1, 18 28. Reuscher, S., Akiyama, M., Mori, C., Aoki, K., Shibata, D., Shiratake, K., 2013. Genome-wide identification and expression analysis of aquaporins in tomato. PLoS One 8, e79052. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S., Mittler, R., 2004. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134, 1683 1696. Sade, N., Moshelion, M., 2017. Plant aquaporins and abiotic stress. In: Chaumont, F., Tyerman, S.D. (Eds.), Plant Aquaporins: From Transport to Signaling. Springer, pp. 185 206. Sade, N., Vinocur, B.J., Diber, A., Shatil, A., Ronen, G., Nissan, H., et al., 2009. Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytol. 181, 651 661. Sade, N., Gebretsadik, M., Seligmann, R., Schwartz, A., Wallach, R., Moshelion, M., 2010. The role of tobacco aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress. Plant Physiol. 152, 245 254.

Plant Life under Changing Environment

660

25. The role of aquaporins during plant abiotic stress responses

Sakurai, J., Ishikawa, F., Yamaguchi, T., Uemura, M., Maeshima, M., 2005. Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol. 46, 1568 1577. Secchi, F., Lovisolo, C., Schubert, A., 2007. Expression of OePIP2;1 aquaporin gene and water relations of Olea europaea twigs during drought stress and recovery. Ann. Appl. Biol. 150, 163 167. Shekhawat, U.K., Ganapathi, T.R., 2013. Overexpression of a native plasma membrane aquaporin for development of abiotic stress tolerance in banana. Plant. Biotechnol. J. 11, 942 952. Siefritz, F., Tyree, M.T., Lovisolo, C., Schubert, A., Kaldenhoff, R., 2002. PIP1 plasma membrane aquaporins in tobacco from cellular effects to function in plants. Plant Cell 14, 869 876. Smith-Espinoza, C., Richter, A., Salamini, F., Bartels, D., 2003. Dissecting the response to dehydration and salt (NaCl) in the resurrection plant Craterostigma plantagineum. Plant Cell Environ. 26, 1307 1315. Sonah, H., Deshmukh, R.K., Labbe, C., Belanger, R.R., 2017. Analysis of aquaporins in Brassicaceae species reveals high-level of conservation and dynamic role against biotic and abiotic stress in canola. Sci. Rep. 7, 2771. Surbanovski, N., Grant, O.M., 2014. The emerging role of aquaporins in plant tolerance of abiotic stress. In: Ahmad, P., Rasool, S. (Eds.), Emerging Technologies and Management of Crop Stress Tolerance, vol. 2. Elsevier, pp. 431 447. Surbanovski, N., Sargent, D.J., Else, M.A., Simpson, D.W., Zhang, H., Grant, O.M., 2013. Expression of Fragaria vesca PIP aquaporins in response to drought stress: PIP down-regulation correlates with the decline in substrate moisture content. PLoS One 8, e74945. Takano, J., Wada, M., Ludewig, U., Schaaf, G., von Wiren, N., Fujiwara, T., 2006. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18, 1498 1509. Tanaka, M., Wallace, I.S., Takano, J., Roberts, D.M., Fujiwara, T., 2008. NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. Plant Cell 20, 2860 2875. Tsuchihira, A., Hanba, Y.T., Kato, N., Doi, T., Kawazu, T., Maeshima, M., 2010. Effect of overexpression of radish plasma membrane aquaporins on water-use efficiency, photosynthesis and growth of eucalyptus trees. Tree Physiol. 30, 417 430. Tyerman, S., Niemietz, C., Bramley, H., 2002. Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ. 25, 173 194. Vandeleur, R.K., Mayo, G., Shelden, M.C., Gilliham, M., Kaiser, B.N., Tyerman, S.D., 2009. The role of plasma membrane intrinsic protein aquaporins in water transport through roots: Diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol. 149, 445 460. Wallace, I.S., Choi, W.G., Roberts, D.M., 2006. The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim. Biophys. Acta Biomembr. 1758, 1165 1175. Wang, L., Li, Q., Lei, Q., Feng, C., Gao, Y., Zheng, X., et al., 2015a. MzPIP2;1: an aquaporin involved in radial water movement in both water uptake and transportation, altered the drought and salt tolerance of transgenic Arabidopsis. PLoS One 10, e0142446. Wang, X., Cai, H., Li, Y., Zhu, Y., Ji, W., Bai, X., et al., 2015b. Ectopic overexpression of a novel Glycine soja stressinduced plasma membrane intrinsic protein increases sensitivity to salt and dehydration in transgenic Arabidopsis thaliana plants. J. Plant. Res. 128, 103 113. Willigen, V.C., Pammenter, N., Mundree, S.G., Farrant, J.M., 2004. Mechanical stabilization of desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does a TIP3;1 and/or compartmentalization of subcellular components and metabolites play a role? J. Exp. Bot. 55, 651 661. Wu, X.N., Rodriguez, C.S., Pertl-Obermeyer, H., Obermeyer, G., Schulze, W.X., 2013. Sucrose-induced receptor kinase SIRK1 regulates a plasma membrane aquaporin in Arabidopsis. Mol. Cell. Proteomics 12, 2856 2873. Xu, Y., Hu, W., Liu, J., Zhang, J., Jia, C., Miao, H., et al., 2014. A banana aquaporin gene, MaPIP1;1, is involved in tolerance to drought and salt stresses. BMC Plant Biol. 14, 59. Xu, W., Dai, W., Yan, H., Li, S., Shen, H., Chen, Y., et al., 2015. Arabidopsis NIP3;1 plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Mol. Plant 8, 722 733. Yamaguchi-Shinozaki, K., Koizumi, M., Urao, S., Shinozaki, K., 1992. Molecular cloning and characterization of 9 cDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: Sequence analysis of one cDNA clone that encodes a putative transmembrane channel protein. Plant Cell Physiol. 33, 217 224.

Plant Life under Changing Environment

References

661

Yamaji, N., Mitatni, N., Ma, J.F., 2008. A transporter regulating silicon distribution in rice shoots. Plant Cell 20, 1381 1389. Yu, Q., Hu, Y., Li, J., Wu, Q., Lin, Z., 2005. Sense and antisense expression of plasma membrane aquaporin bnpip1 from Brassica napus in tobacco and its effects on plant drought resistance. Plant Sci. 169, 647 656. Zangi, R., Filella, M., 2012. Transport routes of metalloids into and out of the cell: a review of the current knowledge. Chem. Biol. Interact. 197, 47 57. Zelazny, E., Borst, J.W., Muylaert, M.L., Batoko, H., Hemminga, M.A., Chaumont, F.O., 2007. FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc. Natl. Acad. Sci. U.S.A. 104, 12359 12364. Zhang, D., Huang, Y., Kumar, M., Wan, Q., Xu, Z., Shao, H., et al., 2017. Heterologous expression of GmSIP1;3 from soybean in tobacco showed growth retardation and tolerance to hydrogen peroxide. Plant Sci. 263, 210 218. Zhao, X.Q., Mitani, N., Yamaji, N., Shen, R.F., Ma, J.F., 2010. Involvement of silicon influx transporter OsNIP2;1 in selenite uptake in rice. Plant Physiol. 153, 1871 1877. Zhou, S., Hu, W., Deng, X., Ma, Z., Chen, L., Huang, C., et al., 2012. Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS One 7, e52439. Zhu, C., Schraut, D., Hartung, W., Scha¨ffner, A.R., 2005. Differential responses of maize MIP genes to salt stress and ABA. J. Exp. Bot. 56, 2971 2981. Zhuang, L., Liu, M., Yuan, X., Yang, Z., Huang, B., 2015. Physiological effects of aquaporin in regulating drought tolerance through overexpressing of Festuca arundinacea aquaporin gene FaPIP2;1. J. Am. Soc. Hortic. Sci. 140, 404 412. Zhuo, C., Wang, T., Guo, Z., Lu, S., 2016. Overexpression of MfPIP2-7 from Medicago falcata promotes cold tolerance and growth under NO3 (-) deficiency in transgenic tobacco plants. BMC Plant Biol. 16, 138.

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C H A P T E R

26 Tolerance mechanisms of medicinal plants to abiotic stresses Hamid Mohammadi1, Saeid Hazrati1 and Mansour Ghorbanpour2 1

Faculty of Agriculture, Azarbaijan Shahid Madani University, Tabriz, Iran 2Department of Medicinal Plants, Faculty of Agriculture and Natural Resources, Arak University, Arak, Iran

26.1 The concept of increased resistance to abiotic stresses in medicinal plants There is no doubt that rapid or gradual environmental changes are the direct threat to agricultural sustainability and food security. Plants have developed different mechanisms to respond to environmental stresses. Short-term changes in environmental factors can lead to cumulative reactions, while gradual changes can lead to adaptation in plants. Individual’s response to environmental stressors depends on many factors such as type and duration of stress and plant species. The exposure of plants to adverse environmental conditions such as extremely high or low temperature, light stress and UV, heavy metals, water shortage, air pollutants, nutrients deficiency, and salt stress results in the generation of reactive oxygen species including superoxide, hydrogen peroxide, and hydroxyl radical (Bahuguna and Jagadish, 2015). Plants have developed a set of different mechanisms for adaptation and survival under severe environmental conditions. The adaptation/and or survival of plants grown under harsh environments cause(s) remarkable variations at the cellular and molecular levels. Among the most critical environmental factors, both temperature and water significantly affect plants geographical distribution and consequently agricultural sustainability in different regions of the world (Chinnusamy et al., 2007). Plants respond to adverse environmental stressors (e.g., drought, salinity, heavy metal, flooding, heat, and UV) by several physiological, biochemical, and molecular variations. For instance, different types of phytochemical compounds are used to overcome abiotic or biotic stresses. However, secondary metabolites act a crucial role in adapting plants to their environment. Plants showed different biochemical reactions to drought, salinity, light, temperature, and heavy metals stress (Holopainen and Gershenzon, 2010). These

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reactions occur at molecular and physiological levels that ultimately affect the amount of phytochemical compounds (Loreto and Schnitzler, 2010; Dangle and Jones, 2001). Medicinal plants limit secondary metabolites biosynthesis to a specific metabolite to survive under stressful conditions. The recent findings showed that plants use different mechanisms to deal with stress conditions, which depend on stressor, time of occurrence, and plant species. Furthermore, research revealed that the molecular, physiological, and biochemical changes in relationships are known to occur during environmental stresses.

26.2 Tolerance to drought stress The medicinal plants quality is defined by the value of their active ingredients, the concentration of these ingredients, and the environmental agents, such as access to water (Ghorbanpour et al., 2013). Drought stress is one of the most significant environmental stresses that restrict the plant’s performance (Wang et al., 2001). The average performance restriction, which is caused by water scarcity, is estimated to be 50% in a global scale. Drought stress manipulates the performance of active and herbal ingredients. AlaviSamani et al. (2015) conducted a study on two species of thymes (Thymus vulgaris and Thymus daenesis). This study indicated that mild drought stress increase the performance of essential oils. Different irrigation levels have a significant effect on the compounds of essential oils, including carvacrol, γ-terpinene, p-cymene, in drought stress plants in comparison with the plants that are not exposed to drought stress. Moreover, a severe drop of thymol amount in T. vulgaris was observed in comparison with T. daenesis. One of the secondary effects of drought stress is reduced accessibility and absorbance of nutrients. This reduced accessibility is considered to be a limitation (Pirzad et al., 2006). The stress caused by water scarcity increase the synthesis of bioactive ingredients. These syntheses are produced by the plant in order to encounter water scarcity (Khan et al., 2011). Drought has a negative impact on plant products and medicinal plants. Naturally, this stress occurs in dry and semidry environments which are presently more prevalent due to the global-warming phenomenon. Drought stress can induce some species-dependent biochemical, physiological, and genetic factors (Zhou et al., 2017). Those plants which are grown in dry environments may dedicate some of the accumulated carbon to the secondary metabolism (Herms and Mattson, 1992). Moreover, drought stress creates a secondary metabolism, called oxidative stress, which reduces the rate of photosynthesis and produces some phenolic compounds. These compounds help the plant in its defensive mechanism (Jaafar et al., 2012). Studies indicated that an increase in polyphenols is caused by phenylalanine ammonia-increase lyase (PAL) and Chalcone synthase (CHS) enzymatic activity (Lattanzio et al., 2009). In other words, production of secondary metabolites, as a defensive mechanism in producer organisms, helps them in their survival against the stress of their environment (Maplestone et al., 1992). For example, the studies which are carried out in drought stress of Salvia officinalis has indicated that stress increases the concentration of terpenes severely (Nowak et al., 2010). In another study, it is indicated that drought stress increases the active ingredient of thymes plant (Mohammadi et al., 2018). In a review by Selmar et al. (2017), it is presented that drought stress increases

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the real biosynthesis of secondary metabolites. The reason for this issue can be a passive shift or activation of specific enzymes in the biosynthesis of natural products.

26.3 Tolerance to salt stress Salinity stress is one of the significant environmental perturbations which restrict plant products all around the world (Wan et al., 2018). The studies indicated that in sensitive plant species, salinity can cause both water reduction and ionic toxicity. It can further cause nutrient deficiency, growth reduction, and even plant death of the plant species. Plants develop different mechanisms in order to encounter salinity stress; these mechanisms regulate the amount of accumulated salt in different tissues. Tolerant plant species, in comparison with sensitive species, can better utilize their protective mechanisms against stress. These mechanisms comprise the distribution of toxic ions between the organs/ tissues or within the cells and osmolytes accumulation which contributes to the photosynthetic activity. Furthermore, induction of antioxidant systems can further contribute to the protection of plants against salinity (Neto et al., 2014; Mittova et al., 2002). The researches indicated that salinity stress inhibits the growth of Aloe vera, Matricaria necati, and T. vulgaris plants (Said-Al Ahl and Omer, 2011; Aziz et al., 2008). It is indicated that salinity reduces the chlorophyll content; this reduction can prevent chlorophyll synthesis and increase chlorophyll degradation. Imbalance in chlorophyll metabolism reduces photosynthesis and, in severe cases, causes necrosis. Studies proved that salinity stress reduces the amount of essential oil contents of some of the plant species, such as mint species (Aziz et al., 2008) and basil (Ashraf and Orooj, 2006). However, in some other species, such as Marjoram, salinity stress increases the value of several essential oil constituents (Baghalian et al., 2008). Moreover, it is observed that salinity stress increases the percentage of the essential oils contents in thymes, basil, and S. officinalis (Baher et al., 2002; Hendawy and Khalid, 2005; Ezz El-Din et al., 2009). But the results indicated different essential oil compounds. For example, in coriander roots, salinity stress increases the amount of carvacrol but decreases the amount of γ-trepine (Neffati and Marzouk, 2008). Studies indicated that an increase in oil gland density along with more gland production during the stress can be a reason for essential oil accumulation in certain medicinal and aromatic plant species. Another reason can be net assimilation or assimilation distribution during the growth and differentiation processes. Sometimes, reduction of primary metabolism during stress causes the accumulation of special interface products; these interface products can shift toward secondary metabolites synthesis, such as essential oil. Secondary metabolites levels are reduced during stress which is related to the general anabolism. Anabolism is prevented in salinity stress conditions (Said-Al Ahl et al., 2016).

26.4 The mechanism of resistance to light stress and UV in medicinal plants Light is a vital factor in photosynthesis by which plants grow and produce food. The light intensity and cumulative light intensity (total radiation during the growing period) are useful in plants growth development. Plant growth is a function of the amount of visible light that forms 40% 50% of the total solar radiation. Light stress is one of the most

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unknown and least studied abiotic stresses in plans. Plants and other organisms that are not able to move are prone to this stress. In plants, one of the most important strategies to protect against light stress is the regulation of secondary metabolites biosynthesis. In this regard, numerous studies have been undertaken and quality and photoperiod of light intensity have been investigated in many plants species (Banerjee and Roychoudhury, 2016). Light is the first source of energy for plants, as well as the most important environmental factor affecting growth, development, and other morphophysiological processes (Ali et al., 2005; Dong et al., 2014; Hazrati et al., 2016). At the first stage the intensity of light affects photosynthesis, which is associated with the accumulation of secondary compounds, especially in medicinal plants. In this context, various studies have been carried out on secondary compounds production. Secondary compounds play vital role in adapting medicinal plants to environmental changes (Ncube et al., 2012). However, plants respond to stressors depending on the stress type, intensity, and time of occurrence as well as stressed organ or tissue (Osbourn et al., 2003). Medicinal plants have developed biochemical mechanisms to protect themselves against light-induced damages. These mechanisms have been found to be an efficient pathway to absorb light safely. One of the most important parts of light is UV light that causes plant damage, reduced gene expression, and photosynthesis. Ultraviolet light is one of the invisible frequencies of sunlight with a wavelength from 10 to 400 nm, which causes damage to plants through reducing gene expression and photosynthesis (Jansen et al., 1998). Extremely high light intensity and UV affect a wide type of secondary compounds such as phenolics, flavonoids, terpenoids, and alkaloids, which act as part of phytochemical intermediates under such conditions (Kazan and Manners, 2011). In many cases, it has been observed that an increase in light intensity has led to an increase in secondary compounds accumulation in the plants; for example, a positive correlation has been reported between light intensity and phenolic compounds. The phenols are one of the most important compounds of secondary metabolites that have different reactions regarding performance and signaling under high light intensity (Banerjee and Roychoudhury, 2016). Phenylpropanoids are one of the most critical compounds that play a significant and selective role in UV absorption without decreasing leaf photosynthesis. Flavonoids and hydroxycinematics are the largest group of phenylpropanoids and are among the polyphenolic compounds and considered as the most valuable secondary metabolites in plants. Also, these compounds are known as a prominent group of natural antioxidants that are observed in most plants organs at higher concentrations, for example, in leaves, flowers, and fruits as color and taste agents. In nature, these are usually found as glycosides (Nijveldt et al., 2001; He and Giusti, 2010). Increase in phenylpropanoid metabolism and value of phenolic compounds may be achieved by applying various environmental agents as a stressor. Flavonoids act as a vital role in protecting against oxidative stress since they can hinder the generation of free oxygen radicals by producing antioxidants including peroxidase (POD) and ascorbic acid (Agati and Tattini, 2010). According to the studies by Noori et al. (2009), flavonoids are among the phytochemical compounds that are made to defend against adverse environmental situations such as intense light, water stress, and pollutants. In fact, these metabolites play a role in the sustainability of the cell membrane as antioxidant molecules.

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The current reports emphasize the role of flavonoids as a defense factor in pants adaptation and resistance (Noori et al., 2009). Since these compositions accumulate in the epidermal cells vacuoles, they absorb UV light very well and thus protect sensitive parts of the leaves, such as photosynthetic tissues (palisade and spongy parenchyma). In some cases, some flavonoid compounds play an antioxidant role against light stress (Tosserams et al., 1996). Over the past two decades, ozone layer destruction as an environmental tragedy has been discussed in many scientific literature. The role of flavonoids in controlling UV light damage in plants has been emphasized in many studies (Tattini et al., 2004). For instance, it has been reported that flavonoids prevent DNA damage by absorbing light with 280 320 nm wavelength (Stapleton and Walbot, 1994). In a study on Zingiber officinale Roscoe, different light intensities were studied. The results showed that the total flavonoid content increases with increasing light intensity (Ma et al., 2010). Similarly, flavonoids have been identified as one of the defense compounds playing a critical role in plants adaptation and resistance against environmental stresses such as UV radiation. In a study a variety of light intensities (10, 30, 60, and 90 μmol/m2/s) were applied on Anoectochilus formosanus; the results showed that the flavonoid content decreased at high and low levels of radiation, whereas the highest flavonoid content was obtained at 60 μmol/m2/s light intensity (Ma et al., 2010). Liu et al. (2015) studied light intensity on grapevine flavonoids (quercetin and kaempferol glycosides) content and found that these compounds increased under high light intensity. UV-B radiation (Norway spruce) (Picea abies) increased flavonoids concentration (Fischbach et al., 1999). Also, UV radiation could increase flavonoids production, total phenol content, and hypericumin Hypericum retusum (Namli et al., 2014). In a study on Cassia angustifolia an increase in light intensity from 25% to 100% could increase the secondary compounds (Raju et al., 2013). However, it has been stated that by decreasing light intensity, the amount of some secondary compounds with carbon (phenol, tannin, and trapin) decreased (Wang et al., 2007), whereas compounds containing nitrogen increased in the leaves (Coelho et al., 2007). In Artemisia annua L., artemisinin production in leaves decreased with decreasing the light intensity and then rose again by increasing light intensity (Wang et al., 2008). In a study on the grapevine, compounds such as stilbenes (cis- and trans-piceid), quercetin-3-O-galactoside, quercetin-3-O-glucoside increased under UV-C stress (Crupi et al., 2013). In a study, UV-B significantly increased vinblastine and vincristine in Catharanthus roseus (Bernard et al., 2009). UV radiation (300 400 nm) increased flavonoid content and enhanced the activity of PAL enzyme in soybean plants, which was associated with lower levels of chlorophyll content in plants (Liang et al., 2006). Moreover, UV (300 400 nm) could increase flavonoids in chickpea (Shiozaki et al., 1999). According to the results so far, it is evident that secondary compounds in medicinal plants are more useful as antioxidants under light stress (Fig. 26.1). Important compounds accumulate under high light intensities and play an essential function in supporting plants against light stress. As can be seen from the figure, xanthophyll cycle plays a significant role in eliminating heat in plants grown under high light intensity. Furthermore, secondary compounds such as glucosinolate would increase under light stress, especially in medicinal plants belonging to Brassicaceae family (Banerjee and Roychoudhury, 2016). In a study on Nasturtium an increase in glycosylated compounds production was observed under high light intensity (Schreiner et al., 2014).

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High Light Stress

Phenolic Compounds

Oxygenated Carotenoids

Sulfur-rich Secondary Metabolites

Combined Roles

ROS Detoxification

Photoprotection

FIGURE 26.1 Secondary metabolites in medicinal plants serve as antioxidants under light stress. Source: Modified from Banerjee, A., Roychoudhury, A., 2016. Plant responses to light stress: oxidative damages, photoprotection, and role of phytohormones. In: Ahammed, G.J., Yu, J.-Q. (Eds.), Plant Hormones Under Challenging Environmental Factors. Springer, pp. 181 213.

Stimulate of Signaling Molecules

In various studies the synthesis of essential oil was observed in medicinal plants under high light intensity. For instance, Salehi and Hazrati (2017) have found that Chamomile plants produce the highest amount of essential oil when light intensity is at its maximum level. Under different light intensities, chemical compounds in Plectranthus amboinicus altered so that a significant increase in sesquiterpenoid was observed due to low light intensity (Noguchi and Amaki, 2016). In a study on Mentha arvensis, various light intensities were investigated, and the findings showed that the intensity of light affects chemical compounds, for instance, the low light intensity increased neomenthol, menthol, and methyl acetate. On the other hand, increases in light intensity could increase limonene synthase, limonene hydroxylase, (2)—isopiperitenol dehydrogenase, (1)—pulegone reductase and menthol dehydrogenase. Also, essential oil percentage significantly increased under high intensity of light (Souza et al., 2015).

26.5 The resistance mechanism of medicinal and aromatic plants to temperature stress The high or low temperatures also limit plants growth and development. Generally, the temperature has a significant effect on medicinal plants distribution. In medicinal plants, morphological features and chemical compounds represent the plant’s growth condition. Optimal temperature helps plants to grow better and complete their life cycle (Naeem et al., 2012). The adverse effects of temperature on plants are severe and create a fundamental problem that often causes damage to crops and reduce yield around the world. Furthermore, about recent global warming scenarios, cultivation of crops and medicinal plants in areas that are not proper has increased the importance of temperature stress. Temperature, as an important environmental factor, affects structural and physiological processes of plant cells as well as their development. The adverse effects of high or low temperatures can occur in all developmental processes and cells structure. The sensitivity of a plants species to temperature is related to their origin. Plants survive adverse environmental

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temperatures through acclimation or adaptation (Lamalakshmi Devi et al., 2017). With change in temperature, morphological, physiological, biochemical, metabolic, and molecular changes in the plants is observed. Under these conditions, plants go through the mechanisms that increase their adaptability and survival (Theocharis et al., 2012).

26.6 Heat stress Heat stress is one of the predominant environmental abiotic stresses that significantly affect plant production. More than 23% of the earth’s surface is subjected to an average annual temperature of 40 C or more. In the United States the average yield of most plants is 3 7 times lower than the expected yield. The heat and drought stress is the primary reason for this reduction. Increasing demand for food prompts plant breeders to breed high-yield plants with resistant to environmental stress. Higher temperature stress leads to physiological, biochemical, and molecular changes and causes damage to proteins and cell membranes to lipids. These damages increase secondary metabolites biosynthesis in plants tissues, which is an indicator of temperature stress (Zobayed et al., 2005). The physiological and molecular viewpoint of heat stress in medicinal and aromatic plants is schematically shown in Fig. 26.2. Increased activity of enzymatic antioxidants, compatible solutes, and secondary metabolites

Decrease in leaf photosynthesis, relative water content

Physiological responses

FIGURE 26.2 Physiological and molecular relations to high temperature in medicinal plants. Source: Modified from Wani, S.H., Kapoor, N., Mahajan, R., 2017. Metabolic responses of medicinal plants to global warming, temperature and heat stress. In: Ghorbanpour, M., Varma, A. (Eds.), Medicinal Plants and Environmental Challenges. Springer International Publishing AG. Available from: https://doi.org/10.1007/978-3-319-68717-9_1.

High temperature stress

Molecular responses

Activation of HSP/molecular chaperone network

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Heat stress strongly limits photosynthesis in plants. Also, protein metabolism changes due to decomposition and denaturation of proteins and inactivation of enzymes. When plants are exposed to temperatures higher than the optimum temperature, natural protein synthesis is prevented. It has been well documented that heat stress increases the amount of a group of proteins, namely, heat shock proteins (Al-Whaibi, 2011). These proteins have been the topic of many studies over the years to investigate their functions and roles (Wani et al., 2017). However, further investigations are still needed. A part of the resistance mechanisms to overcome temperature stress occurs through the production of secondary metabolites that are used for cell homeostasis (Fig. 26.3) Bokszczanin et al. (2013). Temperature has a significant effect on the production of secondary metabolites in plants (Borges et al., 2017). Carotenoids are among the essential compounds playing a role in protecting photosynthesis and stress-signaling pathways. There are several documents reporting chlorophyll reduction due to high-temperature stress (Reda and Mandoura, 2011). It has been found that xanthophyll cycle capacity increases under higher temperatures (Davison et al., 2002). Not only this, the accumulation of flavonoids in medicinal plants increases under higher temperatures to increase resistance. In some cases, accumulation of water-soluble metabolites with a low molecular weight including amino acids and sugars, so-called osmolytes, is considered as one of the most significant resistance approaches against high temperatures in plants, which include amino acids and sugars (Mohammadi et al., 2018). Moreover, increase in biosynthesis of other compounds such as glutathione and ascorbate to improve cellular resistance has been reported (Hatami et al., 2017). Under temperature stress, aromatic amino acids compound, tryptophan, triazine and phenylalanine, which are produced in the Shikimic acid pathway, are responsible for producing secondary metabolism as a result of stressresistance conditions (Suguiyama et al., 2014). Furthermore, temperature stress increases antioxidant enzyme activity including superoxide dismutase, catalase, and POD, to remove reactive oxygen species (Ncube et al., 2012).

High temperature

Stress proteins

Accumulation of Stress Metabolites

Photoprotection Pigments

Combined Functions

Acquired Heat Stress Tolerance

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FIGURE 26.3 The role of proteins, genes, and metabolic compounds in resistance to heat stress. Source: Modified from Bokszczanin, K.L., Solanaceae Pollen Thermotolerance Initial Training Network (SPOT-ITN) Consortium, Fragkostefanakis, S., 2013. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front. Plant Sci. 4, 315.

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Many studies have performed on the impacts of different temperature regime on medicinal plants grown under controlled conditions. For example, high temperature during the growing period of poppy has been found to be directly related to the amount of morphine (McAlister et al., 2016). Also, in many studies, high daytime temperature and low night temperature could increase the amount of active compounds in medicinal plants. In a study on of St. John’s Wort grown under high-temperature (35 C) condition, the content of POD activity and hypericin, pseudohypericin, and hyperforin increased (Zobayed et al., 2005). Increase in the amount of organic and volatile compounds have also been observed in many medicinal plants grown under high-temperature condition (Sharkey and Loreto, 1993; Parker, 1977; Sharkey and Yeh, 2001).

26.7 Cold stress It has been acknowledged that only 12% of the earth’s surface (without ice and snow) can be applied for agricultural practices; therefore most of the plants will be exposed to low-temperature stress (Ramankutty et al., 2008). The drop in temperature usually adversely affects the yield and production of crops. To survive under such unpredictable conditions, plants have created complex mechanisms that make them ale to receive environmental messages and then respond to them. Among abiotic stress, cold stress is one of the most important environmental stresses that have been extensively studied because of the key association with various developmental phenomena and its effect on agricultural production (Rahman, 2013). According to Gusta et al. (2005) and Zhou et al. (2011), cold stress is known as low temperatures but above the freezing point (usually lower than 10 C, based on the plant species) and varies from the freezing temperature generally occurring below zero. The low temperature (cold stress) directly influences plants performance through altering morphophysiological, metabolic, and genetic processes (Ruelland et al., 2009). Variations in structure linked with low temperature include a change in membrane formation, leading to a reduction in the fluidity of the membrane (Sevillano et al., 2009). Also, the rapid generation of reactive oxygen species triggers oxidative stress, which is known as a result of low-temperature stress (Ruelland et al., 2009; Sevillano et al., 2009). Plants are equipped with different enzymatic and nonenzymatic approaches to overcome these stresses to reduce detrimental impacts of cold stress (Ruelland et al., 2009). Fig. 26.3 shows the fundamental responses of plants during cold stress exposure. In nature, plants can tolerate cold stress through a process known as acclimation, as plants are usually exposed to gradual decrease in temperature (Thomashow, 1999). Acclimation to cold stress comprises biochemical mechanisms including alterations in cell membrane composition and integrity (Thomashow, 1999; Miura and Furumoto, 2013; Wisniewski and Gusta, 2014), an increase in soluble compounds in the cells (Wisniewski and Gusta, 2014) structural, and morphological changes as well (Miura and Furumoto, 2013). Studies have shown that all of these processes have messaging networks controlled by plant hormones involved in adapting plants to biotic and abiotic stresses (Peleg and Blumwald, 2011; Shi et al., 2015).

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Many medicinal plants, when exposed to cold stress, increase the amount of biochemical compounds to cold tolerance. During the winter, protective compounds such as sugars (sorbitol, rebitol, inositol), soluble sugars (sucrose, raffineur, trehalose, glucose), low molecular weight nitrogenous substances, such as proline, glycine and betaine, and cold stress phenolic compounds are produced (Griffith and Yaish, 2004; Janska et al., 2010). According to Christie et al. (1994), cold stress is responsible for increasing phenol and related compounds in the cell wall to enhance cold tolerance. Also, an increase in anthocyanins upon exposure to cold stress has been related to cold tolerance (Pennycooke et al., 2005). Christie et al. (1994) reported an increase in biosynthesis of anthocyanin in plants grown under cold stress (Table 26.1).

26.8 Heavy metal stress Heavy metals are the kind of elements with metallic characteristics of flexibility, conductivity, stability, and proprietary ligands with atomic number higher than 20. Although some of these elements are necessary for growth, some plants need little amounts of these elements. In high concentrations, they cause toxicity (Fahimirad and Hatami, 2017). Heavy metals can be found in natural, agricultural, industrial, and urban resources (Orcutt et al., 2000). The studies indicated that stress of heavy metals causes oxidative stresses; they further cause lipid peroxidation, protein denaturation. Plants have two types of activities against heavy metals: avoidance, which prevents the entrance of heavy metals into the plants; and tolerance, by which the plant can continue living with the accumulated heavy metals in its tissues. Those plants which tolerate heavy metals are divided into three groups. The first group is those plants which excluder heavy metals, such as Zinc Violet. The second group includes indicator plants. The absorption of heavy metals in these plants increases linearly with increased concentration of metals in soil, such as Thlaspi, Minuartia, and Armeria. The third group (including Thlaspi caerulescens, Cardaminopsis halleri, and Sedum alfredii) is considered to be hyperaccumulators of heavy metals (Sun et al., 2007). Various mechanisms are reported for reducing the effects of heavy metals, such as combination of metals with organic molecules, phytochelatins, and glutathione. One of the other main defensive mechanisms of plants is biosynthesis induction along with the biosynthesis of secondary compounds including terpenoids, phenylpropanoids, and alkaloids (Mithofer et al., 2004). Different plants indicate various reactions toward heavy metals. For example, in some medicinal plants—like C. roseus—an increase in the amount of cadmium causes an increase in the amount of ajmalcine (Zheng and Wu, 2004). In other medicinal plants such as M. arvensis an increase in the amount of Zn causes an increase in the amount of menthol (Mishra, 1992). Moreover, in Hypericum perforatum, nickel decreased the production and accumulation of hyperforin and hypericin (Murch et al., 2003). Tolerance mechanisms of some medicinal plants to different abiotic stresses was shown in Table 26.1.

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26.8 Heavy metal stress

TABLE 26.1 Abiotic stress Drought

Impact of abiotic stress on some medicinal plants. Plant species

Main findings

References

Thymus vulgaris and Thymus daenesis

Severe drop of thymol amount in T. vulgaris was observed in comparison with T. daenesis

Alavi-Samani et al. (2015)

T. vulgaris and T. daenesis

Severe drop of thymol amount in T. vulgaris was observed in comparison with T. daenesis

Alavi-Samani et al. (2015)

Salvia officinalis

Severe increase in the concentration of terpenes

Nowak et al. (2010)

T. vulgaris

Increase monoterpenes such as thymol, carvacrol, γ-terpinene, and p-cymene

Mohammadi et al. (2018)

Spice and Increases the real biosynthesis of secondary medicinal plants metabolites

Selmar et al. (2017)

Senna (Cassia angustifolia Vahl.)

Increasing sennoside composition with increasing light intensity

Raju et al. (2013)

Perilla frutescens

Increased anthocyanin synthesis

Zhong et al. (1993)

Aloe vera

Anthocyanin accumulation with increased light intensity

Hazrati et al. (2016)

A. vera

High light intensity increased aloin concentration

Hazrati et al. (2016)

Hypericum perforatum

Naphthodianthrones content and phenolic compounds increased under higher light intensity

Raduˇsiene˙ et al. (2012)

Matricaria chamomilla

α-Bisabolol oxide A content accumulates with increase light radiation

Salehi and Hazrati (2017)

Ozone fumigation

Ginkgo biloba

Increased the concentrations of terpenes, decreased the concentrations of phenolics

He et al. (2009)

Salt

Mint species

Reduces the amount of essential oil contents

Aziz et al. (2008)

Basil

Reduces the amount of essential oil contents

Ashraf and Orooj (2006)

Marjoram

Increases the amount of several essential oil compounds

Baghalian et al. (2008)

S. officinalis

Increases the percentage essential oils

Hendawy and Khalid (2005)

Thymes

Increases the percentage essential oils

Ezz El-Din et al. (2009)

Coriander

Increases the amount of carvacrol, but decreases the amount of γ-trepine

Neffati and Marzouk (2008)

Catharanthus roseus

Increase the amount of Ajmalcine

Zheng and Wu (2004)

Mentha arvensis

Increase the amount of menthol

Mishra (1992)

H. perforatum

decreased the production and accumulation of hyperforin and hypericin

Murch et al. (2003)

Light

Heavy metals

(Continued)

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26. Tolerance mechanisms of medicinal plants to abiotic stresses

TABLE 26.1 (Continued) Abiotic stress

Plant species

Main findings

References

Heat

Sorghum

High temperatures could increase the production of phenolics, flavonoids

Wu et al. (2016)

Strawberry

Phenolic acid, flavonols, anthocyanins, and antioxidant capacities with increased temperature

Wang and Zheng (2001)

Eleutherococcus senticosus

Eleutherosides and chlorogenic acid content decreased with decreasing temperature

Shohael et al. (2006)

E. senticosus

Flavonoids and total phenolic increased to growing at 24 C

Shohael et al. (2006)

Polygonum minus

Content of flavonols and flavanols under higher temperature treatment were greater compared to lower temperature

Goh et al. (2015)

H. perforatum

Naphthodianthrones content and phenolic compounds increased under higher temperature and hyperforin content decreased

Raduˇsiene˙ et al. (2012)

Artemisia tilesii

Cold stress has led to decrease of the flavonoids content

Havryliuk et al. (2017)

Arabidopsis thaliana

Low tempera-temperature has been shown to induce anthocyanin synthesis

Choi et al. (2009)

Datura metel

Increased the concentrations of serotonin

Murch et al. (2009)

Pringlea antiscorbutica

Increased levels of polyamines (agmatine and putrescin)

Hummel et al. (2004)

Zea mays

Accumulation of anthocyanins during cold stress increased

Christie et al. (1994)

Cold stress

26.9 Conclusion Although abiotic stresses are among the most critical threats to medicinal plants growth and development, defense mechanisms in medicinal plants have not been well understood yet. When medicinal plants are subjected to abiotic stress, physiological, biochemical, phytochemical and molecular responses are used to cope with stress. Due to climate changes, plants need to enhance their system in response to extreme environmental conditions. One of the most important groups of plants affected by these climatic variations is medicinal plants. Due to having several chemical compounds, these plants are more prone to environmental changes. Therefore understanding the mechanisms by which medicinal plants cope with these stresses is necessary. Also, further studies are needed to understand resistance mechanisms in which chemical compounds play a crucial role.

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References

675

References Agati, G., Tattini, M., 2010. Multiple functional roles of flavonoids in photoprotection. New Phytol. 186, 786 793. Alavi-Samani, S.M., Kachouei, M.A., Pirbalouti, A.G., 2015. Growth, yield, chemical composition, and antioxidant activity of essential oils from two thyme species under foliar application of jasmonic acid and water deficit conditions. Hortic. Environ. Biotechnol. 56 (4), 411 420. Ali, M.B., Hahn, E.J., Paek, K.Y., 2005. Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet. Environ. Exp. Bot. 54, 109 120. Al-Whaibi, M.H., 2011. Plant heat shock proteins: a mini review. J. King Saud Univ. Sci. 23, 139 150. Ashraf, M., Orooj, A., 2006. Salt stress effects on growth, ion accumulation and seed oil concentration in an arid zone traditional medicinal plant ajwain (Trachyspermum ammi [L.] Sprague). J. Arid. Environ. 64 (2), 209 220. Aziz, E.E., Al-Amier, H., Craker, L.E., 2008. Influence of salt stress on growth and essential oil production in peppermint, pennyroyal, and apple mint. J. Herbs Spices Med. Plants 14, 77 87. Baghalian, K., Haghiry, A., Naghavi, M.R., Mohammadi, A., 2008. Effect of saline irrigation water on agronomical and phytochemical characters of chamomile (Matricaria recutita L.). Sci. Hortic. 116, 437 441. Baher, Z.F., Mirza, M., Ghorbanli, M., Rezaii, M.B., 2002. The influence of water stress on plant height, herbal and essential oil yield and composition in Satureja hortensis L. Flavour Fragr. J. 17, 275 277. Bahuguna, R.N., Jagadish, K.S.V., 2015. Temperature regulation of plant phonological development. Environ. Exp. Bot. 111, 83 90. Banerjee, A., Roychoudhury, A., 2016. Plant responses to light stress: oxidative damages, photoprotection, and role of phytohormones. In: Ahammed, G.J., Yu, J.-Q. (Eds.), Plant Hormones Under Challenging Environmental Factors. Springer, pp. 181 213. Bernard, Y.K., Binder, Christie, A.M., Peebles Jacqueline, V., Shanks, K.-Y.S., 2009. The effects of UV-B stress on the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots. Biotechnol. Prog. 25, 8615. Bokszczanin, K.L., Solanaceae Pollen Thermotolerance Initial Training Network (SPOT-ITN) Consortium, Fragkostefanakis, S., 2013. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front. Plant Sci. 4, 315. Borges, C.V., Minatel, I.O., Gomez-Gomez, H.A., Pereira Lima, G.P., 2017. Medicinal plants: Influence of environmental factors on the content of secondary metabolites. In: Ghorbanpour, M., Varma, A. (Eds.), Medicinal Plants and Environmental Challenges. Springer International Publishing AG. Available from: https://doi.org/ 10.1007/978-3-319-68717-9_1. Chinnusamy, V., Zhu, J., Zhu, J.K., 2007. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12, 444 451. Choi, S., Kwon, Y.R., Hossain, M.A., Hong, S., Lee, B., Lee, H., 2009. A mutation in ELA1, an age dependent negative regulator of PAP1/MYB75, causes UV-and cold stress tolerance in Arabidopsis thaliana seedlings. Plant Sci. 176, 678 686. Christie, P.J., Alfenito, M.R., Walbot, V., 1994. Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 4, 541 549. Coelho, G.G., Rachwal, M.F.G., Dedecek, N.A., Curcio, G.R., Nietsche, K., Schenkel, E.P., 2007. Effect of light intensity on methylxanthine contents of Ilex paraguariensis A St. Hil. Biochem. Syst. Ecol. 35, 75 80. Crupi, P., Pichierri, A., Basile, T., Antonacci, D., 2013. Postharvest stilbenes and flavonoids enrichment of table grape cv Redglobe (Vitis vinifera L.) as affected by interactive UV-exposure and storage conditions. Food Chem. 141, 802 808. Dangle, J.L., Jones, J.D.G., 2001. Plant pathogens and integrated defence responses to infection. Nature 411, 826 833. Davison, P.A., Hunter, C.N., Horton, P., 2002. Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418, 203 206. Dong, C., Fu, Y., Liu, G., Liu, H., 2014. Low light intensity effects on the growth, photosynthetic characteristics, antioxidant capacity, yield and quality of wheat (Triticum aestivum L.) at different growth stages in BLSS. Adv. Space Res. 53, 1557 1566. Ezz El-Din, A.A., Aziz, E.E., Hendawy, S.F., Omer, E.A., 2009. Response of Thymus vulgaris L. to salt stress and alar (B9) in newly reclaimed soil. J. Appl. Sci. Res. 5, 2165 2170.

Plant Life under Changing Environment

676

26. Tolerance mechanisms of medicinal plants to abiotic stresses

Fahimirad, S., Hatami, M., 2017. Heavy metal-mediated changes in growth and phytochemicals of edible and medicinal plants. In: Ghorbanpour, M., Varma, A. (Eds.), Medicinal Plants and Environmental Challenges. Springer International Publishing AG. Available from: https://doi.org/10.1007/978-3-319-68717-9_1. Fischbach, R.J., Kossmann, B., Panten, H., Steinbrecher, R., Heller, W., Seidlitz, H.K., et al., 1999. Seasonal accumulation of ultraviolet-B screening pigments in needles of Norway spruce (Picea abies (L.) Karst.). Plant Cell Environ. 1999 (22), 27 37. Ghorbanpour, M., Hatami, M., Khavazi, K., 2013. Role of plant growth promoting rhizobacteria on antioxidant enzyme activities and tropane alkaloids production of Hyoscyamus niger under water deficit stress. Turk. J. Biol. 37, 350 360. Goh, H.-H., Khairudin, K., Sukiran, N.A., Normah, M.N., Baharum, S.N., 2015. Metabolite profiling reveals temperature effects on the VOCs and flavonoids of different plant populations. Plant Biol. 18, 130 139. Griffith, M., Yaish, M.W.F., 2004. Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci. 9, 399 405. Gusta, L.V., Trischuk, R., Weiser, C.J., 2005. Plant cold acclimation: the role of abscisic acid. Journal of Plant Growth Regulation. 24, 308 318. Hatami, M., Hadian, J., Ghorbanpour, M., 2017. Mechanisms underlying toxicity and stimulatory role of singlewalled carbon nanotubes in Hyoscyamus niger during drought stress simulated by polyethylene glycol. J. Hazard. Mater. 324, 306 320. Havryliuk, O., Matvieieva, N., Tashyrev, O., Yastremskaya, L., 2017. Influence of cold stress on growth and flavonoids accumulation in Artemisia tilesii “hairy” root culture. Agrobiodiversity 163 167. Hazrati, S., Tahmasebi-Sarvestani, Z., Modarres-Sanavy, S.A.M., Mokhtassi-Bidgoli, A., Nicola, S., 2016. Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L. Plant Physiol. Biochem. 106, 141 148. He, X., Huang, W., Chen, W., Dong, T., Liu, C., Chen, Z., et al., 2009. Changes of main secondary metabolites in leaves of Ginkgo biloba in response to ozone fumigation. J. Environ. Sci. 21, 199 203. He, J., Giusti, M.M., 2010. Anthocyanins: natural colorants with health-promoting properties. Annu. Rev. Food Sci. Technol. 1, 163 187. Hendawy, S.F., Khalid, Kh.A., 2005. Response of sage (Salvia officinalis L.) plants to zinc application under different salinity levels. J. Appl. Sci. Res. 1, 147 155. Herms, D.A., Mattson, W.J., 1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67, 283 335. Holopainen, J.K., Gershenzon, J., 2010. Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 15, 176 184. Hummel, I., El-Amrani, A., Gouesbet, G., Hennion, F., Coue´e, I., 2004. Involvement of polyamines in the interacting effects of low temperature and mineral supply on Pringlea antiscorbutica (Kerguelen cabbage) seedlings. J. Exp. Bot. 399, 1125 1134. Jaafar, H.Z., Ibrahim, M.H., Fakri, N.F.M., 2012. Impact of soil field water capacity on secondary metabolites, phenylalanine ammonia-lyase (PAL), malondialdehyde (MDA) and photosynthetic responses of Malaysian Kacip Fatimah (Labisia pumila Benth). Molecules 17, 7305 7322. Jansen, M.A.K., Gaba, V., Greenberg, B.M., 1998. Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci. 3, 131 135. Janska, A., Marsik, P., Zelenkova, S., Ovesna, J., 2010. Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol. 12, 395 405. Kazan, K., Manners, J.M., 2011. The interplay between light and jasmonate signalling during defence and development. J. Exp. Bot. 62, 4087 4100. Khan, M.A.M., Ulrichs, C., Mewis, I., 2011. Water stress alters aphid-induced glucosinolate response in Brassica oleracea var. italica differently. Chemoecology 21, 235 242. Lamalakshmi Devi, E., Sudhir Kumar, Basanta Singh, T., Sharma, S.K., Beemrote, A., Premabati Devi, C., et al., 2017. Adaptation strategies and defence mechanisms of plants during environmental stress. In: Ghorbanpour, M., Varma, A. (?ds.), Medicinal Plants and Environmental Challenges. Springer International Publishing AG. Available from: https://doi.org/10.1007/978-3-319-68717-9_1. Lattanzio, V., Cardinali, A., Ruta, C., et al., 2009. Relationship of secondary metabolism to growth in oregano (Origanum vulgare L.) shoot cultures under nutritional stress. Environ. Exp. Bot. 65, 54 62.

Plant Life under Changing Environment

References

677

Liang, B., Huang, X., Zhang, G., Zhang, F., Zhou, Q., 2006. Effect of lanthanum on plants under supplementary ultravio-let-B radiation: effect of lanthanum on flavonoid contents in Soybean seedlings exposed to supplementary ultraviolet-B radiation. J. Rare Earths 24, 613 616. Liu, L., Gregan, S., Winefield, C., Jordan, B., 2015. From UVR8 to flavonol synthase: UV-B-induced gene expression in Sauvignon blanc grape berry. Plant Cell Environ. 38 (5), 905 919. Loreto, F., Schnitzler, J.-P., 2010. Abiotic stresses and induced biogenic volatile organic compounds. Trends Plant Sci. 15, 154 166. Ma, Z., Li, S., Zhang, M., 2010. Light intensity affects growth, photosynthetic capability, and total flavonoid accumulation of anoectochilus plants. Hort Science 45, 863 867. Maplestone, R.A., Stone, M.J., Williams, D.H., 1992. The evolutionary role of secondary metabolites—a review. Gene 115 (1-2), 151 157. McAlister, S., Ou, Y., Neff, E., Hapgood, K., Story, D., Mealey, P., McGain, F., 2016. The Environmental footprint of morphine: a life cycle assessment from opium poppy farming to the packaged drug. BMJ Open. 6 (10), e013302. Mishra, A., 1992. Effect of Zn stress in Japanese mint as related to growth photosynthesis, chlorophyll content and secondary plant products- the mono terpenes. Photosynthetica 26 (2), 225 234. Mithofer, A., Schulze, B., Boland, W., 2004. Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett. 566, 1 5. Mittova, V., Tal, M., Volokita, M., Guy, M., 2002. Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol. Plant. 115, 393 400. Miura, K., Furumoto, T., 2013. Cold signaling and cold response in plants. Int. J. Mol. Sci. 14, 5312 5337. Mohammadi, H., Ghorbanpour, M., Brestic, M., 2018. Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Ind. Crop Prod. 122, 119 132. Murch, S.J., Haq, K., Rupasinghe, H.P.V., Saxena, P.K., 2003. Nickel contamination affects growth and secondary metabolite composition of St. John’s Wort (Hypericum perforatum L.). Environ. Exp. Bot. 49, 251 257. Murch, S.J., Alan, A.R., Cao, J., Saxena, P.K., 2009. Melatonin and serotonin in flowers and fruits of Datura metel L. J. Pineal Res. 47, 277 283. Naeem, U.A., Hashmi, H.N., Shamim, M.A., Ejaz, N., 2012. Flow variation in Astore river under assumed glaciated extents due to climate change. Pak. J. Eng. Appl. Sci. 11, 73 81. Namli, S., I¸sıkalan, C., Akba, F., Toker, Z., Tilkat, E.A., 2014. Effects of UV-B radiation on total phenolic, flavonoid and hypericin contents in Hypericum retusum Aucher grown under in vitro conditions. Nat. Prod. Res. 28, 2286 2292. Ncube, B., Finnie, J.F., Van Staden, J., 2012. Quality from the field: the impact of environmental factors as quality determinants in medicinal plants. South Afr. J. Bot. 82, 11 20. Neffati, M., Marzouk, B., 2008. Changes in essential oil and fatty acid composition in coriander (Coriandrum sativum L.) leaves under saline conditions. Ind. Crops Prod. 28, 137 142. Neto, M.C.L., Lobo, A.K.M., Martins, M.O., Fontenele, A.V., Silveira, J.A.G., 2014. Dissipation of excess photosynthetic energy contributes to salinity tolerance: a comparative study of salt-tolerant Ricinus communis and saltsensitive Jatropha curcas. J. Plant Physiol. 171, 23 30. Nijveldt, R.J., van Nood, E., van Hoorn, D.E., Boelens, P.G., van Norren, K., van Leeuwen, P.A., 2001. Flavonoids: a review of probable mechanisms of action and potential applications. Am. J. Clin. Nutr. 74 (4), 418 425. Noguchi, A., Amaki, W., 2016. Effects of light quality on the growth and essential oil production in Mexican mint. Acta Hortic. 1134, 239 244. Noori, M., Chehreghani, A., Kaveh, M., 2009. Lavonoids of 17 species of Euphorbia, (Euphorbiaceae) in Iran. Toxicol. Environ. Chem. 91 (4), 631 641. Nowak, M., Manderscheid, R., Weigel, H.-J., Kleinwa¨chter, M., Selmar, D., 2010. Drought stress increases the accumulation of monoterpenes in sage (Salvia officinalis), an effect that is compensated by elevated carbon dioxide concentration. J. Appl. Bot. Food Qual. 83, 133 136. Orcutt, D.M., Nilsen, E.T., Hale, M.G., 2000. The Physiology of Plants Under Stress: Soil and Biotic Factors. John Wiley & Sons, Inc, Hoboken, NJ. Osbourn, A.E., Qi, X., Townsend, B., Qin, B., 2003. Dissecting plant secondary metabolism constitutive chemical defences in cereals. New Phytol. 159, 101 108.

Plant Life under Changing Environment

678

26. Tolerance mechanisms of medicinal plants to abiotic stresses

Parker, J., 1977. Phenolics in black oak bark and leaves. J. Chem. Ecol. 3, 489 496. Peleg, Z., Blumwald, E., 2011. Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 14, 290 295. Pennycooke, J.C., Cox, S., Stushnoff, C., 2005. Relationship of cold acclimation, total phenolic content and antioxidant capacity with chilling tolerance in petunia (Petunia 3 hybrida). Environ. Exp. Bot. 53, 225 232. Pirzad, A., Alyari, H., Shakiba, M.R., Zehtab-Salmasi, S., Mohammadi, A., 2006. Essential oil content and composition of German chamomile (Matricaria chamomilla L.) at different irrigation regimes. J. Agron. 5 (3), 451 455. ˇ 2012. Effect of external and internal factors on secondary metabolites ˙ J., Karpaviˇciene, ˙ B., Stanius, Z., Raduˇsiene, accumulation in St. John’s Worth. Bot. Lithuanica 18 (2), 101 108. Rahman, A., 2013. Auxin: a regulator of cold stress response. Physiol. Plant. 147, 28 35. Raju, S., Shah, S., Gajbhiye, N., 2013. Effect of light intensity on photosynthesis and accumulation of sennosides in plant parts of senna (Cassia angustifolia Vahl.). Indian J. Plant Physiol. 18, 285 289. Ramankutty, N., Evan, A.T., Monfreda, C., Foley, J., 2008. Farming the planet: 1. Geographic distribution of global agricultural lands in the year 2000. Global Biogeochem. Cycles 22, 1 19. Reda, F., Mandoura, H.M.H., 2011. Response of enzymes activities, photosynthetic pigments, proline to low or high temperature stressed wheat plant (Triticum aestivum L.) in the presence or absence of exogenous proline or cysteine. Int. J. Acad. Res. 3, 108 115. Ruelland, E., Vaultier, M.N., Zachowski, A., Hurry, V., 2009. Cold Signaling and Cold Acclimation in Plants, first ed Elsevier, Amsterdam. Said-Al Ahl, H.A.H., Omer, E.A., 2011. Medicinal and aromatic plants production under salt stress. A review. Herba Pol. 57, 72 87. Said-Al Ahl, H.A.H., Abou-Ellail, M., Omer, E.A., 2016. Harvest date and genotype influences growth characters and essential oil production and composition of Petroselinum crispum plants, J. Chem. Pharm. Res., 8. pp. 992 1003. Salehi, A., Hazrati, S., 2017. How essential oil content and composition fluctuate in German chamomile flowers during the day? J. Essent. Oil Bear. Plants 20 (3), 622 631. Schreiner, M., Martı´nez-Abaigar, J., Just, G., Jansen, M., 2014. UV-B induced secondary plant metabolites: potential benefits for plant and human health. Biophotonics 2, 34 37. Selmar, D., Kleinwa¨chter, M., Abouzeid, S., Yahyazadeh, M., Nowak, N., 2017. The impact of drought stress on the quality of spice and medicinal plants. In: Ghorbanpour, M., Varma, A. (Eds.), Medicinal Plants and Environmental Challenges. Springer International Publishing AG. Available from: https://doi.org/10.1007/ 978-3-319-68717-9_1. Sevillano, L., Sanchez-Ballesta, M.T., Romojaro, F., Flores, F.B., 2009. Physiological, hormonal and molecular mechanisms regulating chilling injury in horticultural species. Postharvest technologies applied to reduce its impact. J. Sci. Food Agric. 89, 555 573. Sharkey, T.D., Loreto, F., 1993. Water-stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of Kudzu leaves. Oecologia 95, 328 333S. Sharkey, T.D., Yeh, S.S., 2001. Isoprene emission from plants. Annu. Rev. Plant Phys. Plant Mol. Biol. 52, 407 436. Shi, Y., Ding, Y., Yang, S., 2015. Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiol. 56, 7 15. Shiozaki, N., Hattori, I., Gojo, R., Tezuka, T., 1999. Activation of growth and nodulation in symbiotic system between pea plants and leguminous bacteria by near UV radiation. J. Photochem. Photobiol. B: Biol. 50, 33 37. Shohael, A.L.M., Ali, M.B., Yu, K., Hahn, E., Paek, K., 2006. Effect of temperature on secondary metabolites production and antioxidant enzyme activities in Eleutherococcus senticosus somatic embryos. Plant Cell Tissue Organ Cult. 85, 219 228. Souza, M.A.A.D., Santos, L.A.D., Brito, D.M.C.D., Rocha, J.F., Castro, R.N., Fernandes, M.S., et al., 2015. Influence of light intensity on glandular trichome density, gene expression and essential oil of menthol mint (Mentha arvensis L.). J. Essent. Oil Res. 2, 138 145. Stapleton, A., Walbot, v, 1994. Flavonoids protect maize DNA from UV damage. Plant Physiol. 105, 881 889. Suguiyama, V.F., Silva, E.A., Meirelles, S.T., Centeno, D.C., Braga, M.R., 2014. Leaf metabolite profile of the Brazilian resurrection plant Barbacenia purpurea Hook. (Velloziaceae) shows two time-dependent responses during desiccation and recovering. Front. Plant Sci. 5, 96. Sun, Q., Ye, Z.H., Wang, X.-R., Wong, M.H., 2007. Cadmium hyper accumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyper accumulator Sedum alfredii. J. Plant Physiol. 164, 1489 1498.

Plant Life under Changing Environment

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Tattini, M., Galardi, C., Pinelli, P., Massai, R., Remorini, D., Agati, G., 2004. Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytol. 163, 547 561. Theocharis, A., Cle´ment, C., Barka, A.E., 2012. Physiological and molecular changes in plants grown at low temperatures. Planta (2012) 235, 1091 1105. Thomashow, M.F., 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999 (50), 571 599. Tosserams, M., Paisdesa, A., Rozema, J., 1996. The effect of solar UV radiation on four plant species occurring in a coastal grassland vegetation in The Netherlands. Physiol. Plant. 97, 731 739. Wan, S., Wang, W., Zhou, T., Zhang, Y., Chen, J., Xiao, B., et al., 2018. Transcriptomic analysis reveals the molecular mechanisms of Camellia sinensis in response to salt stress. Plant Growth Regul. 84, 481 492. Wang, W.X., Vinocur, B., Shoseyov, O., Altman, A., 2001. Biotechnology of plant osmotic stress tolerance: physiological and molecular considerations. Acta Hortic. 560, 285 292. Wang, M.L., Jiang, Y.S., Wei, J.Q., et al., 2008. Effects of irradiance on growth, photosynthetic characteristics, and artemisinin content of Artemisia annua L. Photosynthetica 46, 17. Wang, M.L., Jiang, Y.S., Wei, J.Q., Wei, X., Qi, X.X., Jiang, S.Y., et al., 2007. Effects of irradiance on growth, photosynthetic characteristics, and artemisinin content of Artemisia annua L. Photosynthetica 46, 17 20. Wang, S.Y., Zheng, W., 2001. Effect of plant growth temperature on antioxidant capacity in strawberry. J. Agric. Food Chem. 49, 4977 4982. Wani, S.H., Kapoor, N., Mahajan, R., 2017. Metabolic responses of medicinal plants to global warming, temperature and heat stress. In: Ghorbanpour, M., Varma, A. (Eds.), Medicinal Plants and Environmental Challenges. Springer International Publishing AG. Available from: https://doi.org/10.1007/978-3-319-68717-9_1. Wisniewski, M., Gusta, L.V., 2014. The biology of cold hardiness: adaptive strategies. Environ. Exp. Bot. 106, 1 3. 2014. Wu, G., Johnson, S.K., Bornman, J.F., Bennett, S.J., Clarke, M.W., Singh, V., et al., 2016. Growth temperature and genotype both play important roles in sorghum grain phenolic composition. Sci. Rep. 6, 21835. Available from: http://dx.doi.org/10.1038/srep21835. Zheng, Z., Wu, M., 2004. Cadmium treatment enhances the production of alkaloid secondary metabolites in Catharanthus roseus. Plant Sci. 166, 507 514. Zhong, J.J.T., Seki, S.I., Kinoshita, S., Yoshida, T., 1993. Effect of light irradiation on anthocyanin production by suspended culture of Perilla frutescens. Biotechnol. Bioeng. 38, 653 658. Zhou, R., Yu, X., Ottosen, C.-O., et al., 2017. Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol. 17, 24. Zhou, M.Q., Shen, C., Wu, L.H., Tang, K.X., Lin, J., 2011. CBF-dependent signaling pathway: a key responder to low temperature stress in plants. Crit. Rev. Biotechnol. 2011 (31), 186 192. Zobayed, S.M.A., Afreen, F., Kozai, T., 2005. Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in St. John’s Wort. Plant Physiol. Biochem. 43, 977 984.

Further reading Corell, M., Garcia, M.C., Contreras, J.I., Segura, M.L., Cermeno, P., 2012. Effect of water stress on Salvia officinalis L. bioproductivity and its bioelement concentrations. Commun. Soil Sci. Plant Anal. 43 (1 2), 419 425. Jing, Y.D., He, Z.L., Yang, X.E., 2007. Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J. Zhejiang Univ. Sci. B 8 (3), 192 207. Misra, A., 1992. Effect of zinc stress in Japanese mint as related to growth, photosynthesis, chlorophyll content and secondary plant products-the monoterpenes. Photosynthetica 26, 225 234. Selmar, D., Kleinwachter, M., 2013. Influencing the product quality by deliberately applying drought stress during the cultivation of medicinal plants. Ind. Crops Prod. 42, 558 566.

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27 Regulation of the Calvin cycle under abiotic stresses: an overview Sonika Sharma1, Juhie Joshi2, Sunita Kataria3, Sandeep Kumar Verma4, Soumya Chatterjee1, Meeta Jain3, Kratika Pathak3, Anshu Rastogi5 and Marian Brestic6 1

Defence Research Laboratory, Tezpur, India 2Plant Science Department, Macdonald Campus, McGill University, Montreal, QC, Canada 3School of Biochemistry, Devi Ahilya University, Indore, India 4Institute of Biological Science, SAGE University, Indore, India 5Laboratory of Bioclimatology, Department of Ecology and Environmental Protection, Poznan University of ´ Poland 6Department of Plant Physiology, Slovak University of Life Sciences, Poznan, Agriculture, Nitra, Slovak Republic

27.1 Introduction Worldwide climate alteration exaggerates the incidence and severity of abiotic stresses that severely influence the growth and development of plants, particularly plant photosynthesis. Plants are sessile organisms, so they are frequently exposed to combination of abiotic stresses that enforce various harmful effects and lead to a tremendous loss of plant yields. Abiotic stresses, such as low temperature, salinity, drought, heat, UV-B, ozone, and exposure to heavy metals, are accountable for drastic crop yield losses (Mahajan and Tuteja, 2005). Stress can be described as an unfavorable condition that causes hindrance in the normal performance and the development of a biological organism such as plants (Levitt, 1980; Jones and Jones, 1989). Abiotic stresses can be responsible for the reduction in photosynthesis and crop productivity (De Oliveira et al., 2013). Photosynthesis is a key physiological phenomenon in plants to regulate the energy flow to enhance carbon fixation and prevent light-induced damage. Two major processes are involved in photosynthesis: electron transport chain dependent on light, and the carbon fixation cycle or the Calvin Benson Bassham cycle. The direct effect of abiotic stresses on photosynthesis is the disturbance in machinery of photosynthesis such as photosystem I (PSI) and

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photosystem II (PSII), transport of electrons, carbon fixation, adenosine triphosphate (ATP) generating system, Calvin cycle, and stomatal conductance. This chapter discusses the current understanding and signifies the regulation of the Calvin Benson Bassham cycle under abiotic stresses.

27.1.1 The Calvin Benson Bassham cycle The Calvin cycle is also known as a reductive pentose phosphate cycle that occurs in the stroma of chloroplast of eukaryotic photosynthates and cytosol of prokaryotic organisms. Benson and Calvin (1950) discovered this cycle in the University of California, Berkeley. In 1961, the Nobel Prize was awarded to Calvin for his work. A three-carbon compound glyceraldehyde 3-phosphate (GAP) is the principal product of this cycle. For the synthesis of sugars, this compound is used as a preliminary material. High-energy compounds such as ATP and reduced nicotinamide adenine dinucleotide phosphate (NADPH) are the two major products of light-dependent reactions. Chlorophyll and the enzymes involved in the synthesis of ATP and NADPH are linked with thylakoid membranes in chloroplasts. After formation, ATP and NADPH are released into the chloroplast stroma. The Calvin cycle takes place in this solution, using the ATP and NADPH molecules as a basis of energy to drive the reduction of carbon dioxide to GAP in Calvin cycle, where they act as a source of energy. The overall reaction that occurs in the Calvin cycle is as follows. 1. Carboxylation Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) catalyzes the carboxylation of ribulose-1,5-bisphosphate (RuBP) as it is a primary CO2 acceptor derived from phosphogluconate (Fig. 27.1) pathway. The activity of RuBisCO is regulated by CO2, O2, Mg21, and pH. 2. Reduction

FIGURE 27.1 Overall carboxylation in the Calvin cycle. Source: Modified from Heineke, D., Scheibe, R., 2009. Photosynthesis: the calvin cycle. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd, Chichester. Available from: https://doi.org/10.1002/ 9780470015902.a0001291.pub2.

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FIGURE 27.2 Overall reductions in the Calvin cycle. Source: Modified from Heineke, D., Scheibe, R., 2009. Photosynthesis: the calvin cycle. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd, Chichester. Available from https://doi.org/10.1002/9780470015902.a0001291.pub2.

In this phase, six molecules of 3-phosphoglycerate (3-PG) are phosphorylated at the expense of six ATP to form glycerate-1,3-bisphoshate. Furthermore, the reduction of six molecules of GAP by NADP-glyceraldehyde-3-phosphate dehydrogenase results in the formation of GAP (Fig. 27.2). 3. Regeneration To continue the fixation of CO2, RuBP must be regenerated. The net production of carbon in the Calvin cycle is one molecule of GAP. Thus from 6 molecules of GAP, three molecules of RuBP are regenerated (Fig. 27.3). The Calvin cycle demonstrates carboxylation and regeneration phase with its enzymes (ribose-5-phosphate isomerase—RPI; phosphoribulokinase—PRK; RuBisCO; phosphoglycerate kinase—PGK; glyceraldehyde-3-phosphate dehydrogenase—GAPDH; triose-phosphate isomerase—TPI; fructose-bisphosphate aldolase—FBA; fructose bisphosphatase—FBPase; transketolase—TKL; sedoheptulose-bisphosphatase—SBPase; ribulose-5-phosphate 3-epimerase—RPE). 27.1.1.1 Calvin cycle enzymes Calvin cycle is operated by 11 different enzymes that catalyze 13 reactions. The “key” regulatory enzymes are RuBisCO, FBPase, SBPase, and PRK. These enzymes play a major role as they control the rate of CO2 fixation. These are as follows. 1. RuBisCO The most abundant enzyme on the earth is RuBisCO (EC 4.1.1.39) (Feller et al., 2008a, b). RuBisCO is a plentiful protein present in living photosynthesizing cells that catalyze the carboxylation of RuBP (Ellis, 1979). The enzyme consists of two types of protein subunits, that is, large units (L, 55 kDa) and small units (S, 13 kDa). This chain combines to form a large complex of 540,000 Da containing eight large chains and eight small chains. Studies suggest that RuBisCO does not limit photosynthetic capacity under a wide range but limits the uptake of carbon from the atmosphere (von Caemmerer, 2000). 2. FBPase FBPase changes the fructose-1,6-bisphosphate into fructose 6-phosphate. It catalyzes the reverse reaction by phosphofructokinase. Its motif (Asp-Pro-Ile/Leu-Asp-Gly/SerThr/Ser) is analogous to that of iositol-1-phosphatase (IMPase), inositol polyphosphate

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FIGURE 27.3 The Calvin cycle demonstrating carboxylation and regeneration phase with their enzymes. FBA, Fructose-bisphosphate aldolase; FBPase, fructose bisphosphatase; GADPH, glyceraldehyde-3-phosphate dehydrogenase; PGK, phosphoglycerate kinase; PRK, phosphoribulokinase; RPE, ribulose-5-phosphate 3-epimerase; RPI, ribose-5-phosphate isomerase; RuBisCO, ribulose-1,5-bisphosphate carboxylase/oxygenase; SBPase, sedoheptulose-bisphosphatase; TKI, triosephosphate isomerase; TKL, transketolase. Source: Modified from Martin, W., Schnarrenberger, C., 1997. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32, 1 18

1-phosphatase (IPPase). Studies by Kossmann et al. (1994) suggested that photosynthesis remains unaffected unless the FBPase activity is less than 34% of wild type species. Moreover, photosynthetic carbon fixation was also insensitive to reductions in the levels of PRKase activity. 3. SBPase SBPase is a homodimeric protein and is about 92,000 Da. The activity of SBPase is governed by a disulfide bond between two cysteine residues and magnesium (Mg21) ion. It is found on the stroma-facing side of the thylakoid membrane in the chloroplast. Studies suggest that a small decrease in SBPase activity reduces photosynthetic activity and carbohydrate levels. Growth analysis of SBPase reveals that shoot, leaf, and floral biomass decline linearly in response to reduced SBPase activity. Bryant (2000) observed that there is a biphasic response of leaf and stem morphology in plants toward decreased SBPase activity. According to their study, it reveals that plants with large reductions in SBPase activity have the same height or are taller than wild type plants but are reported to have thin stems and increased specific leaf area. This was similar to alteration in leaf and stem morphology that takes place in some species as a response to the light environment (Bjo¨rkman, 1981; Evans, 1996). 4. PRK PRK belongs to transferase family, specifically shifting phosphorus-containing groups to an alcohol group acceptor. It catalyzes the ATP-dependent phosphorylation Plant Life under Changing Environment

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of ribulose-5-phosphate (RuP) into RuBP. Till date, class-I and class-II PRK enzymes have been identified (Tabita, 1994; Brandes et al., 1996). The most studied class of PRK is an octamer of approximately 30 kDa subunits present in photosynthetic proteobacteria, whereas, in cyanobacteria (a tetramer) and higher plants (a dimer), it is reported to be approximately 40 kDa subunits (Tabita, 1988, 1994). PGK PGK is the only enzyme of the Calvin cycle that is active as a monomer and is about 44 kDa. It catalyzes reversible transfer of a phosphate group from 1,3bisphosphoglycerate (1,3-BPG) to ADP producing 3-PG and ATP. The enzyme comprises two equal sized domains corresponding to N- and C-terminal of protein. The size of these domains ranges up to 415-monomer residue. 3-PG binds to the Nterminal, whereas the nucleotide substrates, Mg-ATP or Mg-ADP, bind to the Cterminal domain of PGK. GADPH GADPH is a tetramer consisting of 37 kDA subunits that catalyze the conversion of 1,3-BPG to GADPH. Class-I and class-II GAPDH are identified, which share only 15% 20% sequence identity. TPI TPI is a homodimer of approximately 27 kDa subunits in eubacteria, the eukaryotic cytosol, and higher plant chloroplasts that catalyze the reversible interconversion of the triose-phosphate isomers dihydroxyacetone phosphate (DHAP) and Dglyceraldehyde 3-phosphate. On the other hand, hyperthermophilic archaebacteria TPI is a homotetramer of 25 kDa subunits (Kohlhoff et al., 1996). Like PGK, class-I/class-II forms of the enzyme have not been described nor have ancient eubacterial gene duplications/families been proposed. Fructose-1,6-bisphosphate aldolase FBA performs an aldol reaction or reverses the aldol reaction leaving aldol to form sialic acid. In the Calvin cycle, FBA catalyzes a reversible reaction that splits the aldol FBPase into the triose phosphates GAP and DHAP. It can also form DHAP from fructose 1-phosphate and SBPase. It consists of two classes, that is, class-I FBAs (homotetramers) and class-II FBAs (homodimers). The monomers of class-I and class-II FBA share no detectable sequence similarity, but the subunit size of both classes of FBA enzymes is approximately 40 kDa. Transketolase In the Calvin cycle, TKL catalyzes the reverse reaction, the conversion of sedoheptulose-7-P and glyceraldehyde-3-P to pentoses to D-ribose-5-phosphate (aldose) and D-xylulose-5-P (ketose). This enzyme is essential to both the Calvin cycle of higher plants and the oxidative PPP (pentose phosphate pathway). In spinach, both the Calvin cycle and the regenerative segment of the oxidative pentose pathway are localized in plastids where a single isomer of TKL enzyme is functional in both pathways (Martin and Schnarrenberger, 1997). RPE RPE is a homodimer of approximately 23 kDa subunits in animals, eubacteria, and plants. It is a metalloprotein that catalyzes the interconversion between D-ribulose 5phosphate and D-xylulose 5-phosphate. In spinach leaves, RPE is found only in the

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chloroplast with no detectable cytosolic activity (Schnarrenberger et al., 1995). No class-I/class-II enzymes have been described for RPE. 11. Ribose-5-phosphate isomerase RPI belongs to the class of isomerases that catalyze the interconversion of isomers, ribose-5-phosphate (R5P), and ribulose-5-phosphate (Ru5P). It is a homodimer of approximately 23 kDa subunits in most source studies (Hove-Jensen and Maigaard, 1993; Martin et al., 1996b).

27.2 Regulation of the Calvin cycle and its enzymes under abiotic stresses Abiotic stress on plants can be defined as a condition in which abiotic factors hamper the plants from achieving its maximum growth and reproductive potential. Abiotic stresses such as drought, salinity, cold, high temperature, UV-B, ozone, and heavy metals negatively affect the growth, photosynthesis, and productivity of plants. Therefore, an overview of the effect of these stresses is presented especially on the Calvin cycle of the photosynthesis and its related enzymes, and their regulation in the plants. In any stress situation, a plant counters and adapts by compensating, either by slowing down its metabolic activities especially biosynthesis, which in turn affects overall growth and yield, or by utilizing the stored food in the form of starch (Ha et al., 2014).

27.2.1 Water stress A plant faces different kinds of abiotic stresses during its whole life cycle. Of these, water stress is the limiting factor that imparts deleterious effect on growth and yield, especially in breeding crops. Decrease in crop yield under drought conditions has been stated for many economically important crops such as soybean (Frederick et al., 2001), cotton (Pettigrew, 2004), pearl millet (Yadav et al., 2004), and maize (Cattivelli et al., 2008). The processes employed to manage drought conditions by the plant are an interesting area of research. The term “drought resistance” belongs to plant species that has developed adaptability for drought. There are many ways to counter against drought conditions. Of these, “drought escape” is one in which plants complete their vegetative and reproductive growth before an onset of drought. Drought escapers have accelerated metabolic rate, with regard to cell division and expansion for rapid plant development. They also have open stomata which facilitate gas exchange at high rates for an efficient, basic process such as photosynthesis. Photorespiration is a water-use efficiency (WUE) under water limiting condition and assumes a very high metabolic rate, resulting in progressive cell expansion and division (Shavrukov et al., 2017), whereas the other is drought avoidance in which a plant develops “succulent strategy” and manages to store water (high WUE) in the higher tissue irrespective of soil water content and decelerates its metabolic activities to slow down the rate of photosynthesis with small or closed stomata (Fang and Xiong, 2015). Furthermore, some plants develop tolerance in response to drought by modifying or adapting to low tissue water content and maintenance of cell turgor through osmotic adjustment which helps in cellular elasticity and brings increasing protoplasmic resistance

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(Basu et al., 2016). Hence, the WUE parameter is considered an important role in the selection of a trait for breeding and for the improvement of crops in water limiting conditions as it is a major limiting factor for plant productivity in many crops. Furthermore, the response of plants under water limiting conditions is an important aspect of research as it is not confined to arid/semiarid regions; even outside challenge of survival remains the same for the plant and shares the same stress that either belongs to forest of temperate region or (Law et al., 2000; Wilson et al., 2001), or rainforest of tropical (Grace, 1999). In addition, due to anthropogenic activities and rapid change in global environment, water availability is becoming a critical factor for the latter (Fischer et al., 2001). Water availability to plants depends upon the rainfall, water holding capacity of soil, and depth of the water table. Plants contain a large portion of water as cellular volumes, and near about 97% of water gets transpired; only 2% is used by plants for their cell expansion, whereas near 1% is used by plants for their metabolic activities (Taiz and Zeiger, 2014). Decrease in relative water content (RWC) in plants results in many physiological and morphological changes. Moreover, the magnitude of water stress depends on the leaf growing stage and conditions, for example, younger leaves show more resistant to drought and adapt more quickly than the older ones (Chaves, 1991). Under water limiting conditions, RWC in leaves decreases and cell dehydration occurs, which results in the decrease of water potential (Ψ) in the apoplast causing reduction in pressure potential (Ψ p). Moreover, plants close their stomata to prevent further lowering of water potential by transpiration of water and eventually decrease stomatal conductance (gs) which in turn slows down the CO2 assimilation (A) which cannot be reversed by supplying or increasing external CO2 (Lawlor, 2002). CO2 unavailability further downregulates various genes involved in photosynthesis and for the progress of dark reaction (Osakabe and Osakabe, 2012). Closure of stomata is believed to decrease both photosynthetic rate and internal CO2 concentration in leaf (Ci) which further inhibits various mesophyll metabolisms, including the Calvin cycle that also gets affected (Cornic, 2000). Furthermore, this decrease in carbon gain counts for the loss of yield under drought. Moreover, the fall in RWC in water stress conditions affects ATP synthesis by slowing down an important coupling factor—ATP synthesis (Lawlor, 2002; Flexas et al., 2004; Singh et al., 2014). The impaired ATP synthesis is a result of decrease in the electron transport rate (J) (Galme´s et al., 2007). Less availability of ATP for the Calvin cycle affects generation of RuBP and hence affects CO2 fixation rate (Perdomo et al., 2017). In drought conditions, photosynthesis decreases due to the less quantity of RuBP (Carmo-Silva et al., 2010). Moreover, photosynthetic rate in both C3 and C4 plants is directly correlated with RWC and water potential (Ψ) (Lawlor, 2002). It has also been observed that in chloroplast, water stress provokes the generation of reactive oxygen species (ROS) then antioxidants and enzymes that further cause oxidative damage to biomolecules and cellular components (Fu and Huang, 2001; Reddy et al., 2004). This accumulation of ROS in the cell damages ATP synthase (Lawlorand Tezara, 2009). According to Pinheiro and Chaves (2011), plants in water-deficit conditions stimulate a complex network of interactions involving many metabolic events among sugars, ROS, and hormones. Abscisic acid (ABA) has an important role in stomatal opening in water limiting conditions. Along with ABA, other plant hormones either act antagonistically (auxin, cytokinin, or ethylene) or in sync (brassinosteroids, jasmonates, and salicylic acid) to ABA.

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Photosynthesis is a multistep prime process interconnected with several biological pathways in plants (Nouri et al., 2015). Both electron transport chains and CO2 fixation processes depend on the water status. Under drought stress, the photosynthetic pigments and utilization of captured energy in chloroplast reduce. The excess light energy can participate in photoinhibition by affecting the quantum yield of PSII. As a consequence, the Calvin Benson cycle enzymes get inhibited and the process of photorespiration and H2O2 production start (Fu and Huang, 2001; Ort and Baker, 2002; Sanda et al., 2011). Moreover, the syntheses of starch and sucrose also get affected by water limitation condition hence have a vital role in grain filling. The participating enzymes for starch synthesis are adenosine diphosphate glucose pyrophosphorylase, starch synthase, sucrose synthase (SS), and other related enzymes (Taiz and Zeiger, 2006). As per the report, in wheat, water stress downregulates the expression of SS, which affects the rate of grain growth; however, the inactivation of ADP-glucosepyrophosphorylase (ADP-Gppase) in drought conditions stops the growth of grain (Ahmadi and Baker, 2001). During water limiting condition in soil, the diffusion of atmospheric CO2 toward carboxylation site decreases and the net photosynthesis rate and leaf net carbon uptake decrease, which triggers the channelizing of photoassimilates toward root for the maintenance of root growth and yield a higher root-to-shoot ratio (Sharp, 2002). Inhibition of photosynthesis under drought conditions depends on severity, duration of exposure to drought (Miyashita et al., 2005; Flexas et al., 2006). Based on the severity of drought, the recovery process takes place in two stages: after adding water to plants, in the initial few hours; the plant restores its water potential and reopens stomata (Pinheiro et al., 2005; Antonio et al., 2008; Hayano-Kanashiro et al., 2009); and at the later stages plants restart synthesizing photosynthetic proteins (Kirschbaum, 1988). For instance rewatering of cucumber seedlings in water-deficit conditions for several days with a decreased activity of RuBisCO due to the decrease in stomatal conductance and CO2 assimilation started synthesizing RuBisCO protein for photosynthesis recovery (Zhang et al., 2013). In the thylakoid membrane of chloroplast cells, the capture of photon causes the excitation of photosystems in “Z” scheme that causes the evolution of O2 and the generation of NADPH used in the Calvin Benson cycle to reduce CO2. The electrochemical proton gradient (DpH) generates by the transfer of electrons and protons in lumen, helping in ATP synthesis by ATP synthase (coupling factor, CF1 CF0). Both ATP and NADPH are utilized during the Calvin Benson cycle to synthesize RuBP and to reduce the atmospheric CO2 catalyzed by RuBisCO. In C3 plants, RuBisCO adds maximum portion of soluble leaf proteins (approximately 50%) (Spreitzer and Salvucci, 2002); however, in C4 plants, it accounts for approximately 30% (Sugiyama et al., 1984). Furthermore, in C3 plants, RuBisCO contributes up to 20% 30% of total leaf nitrogen, and 5% 9% in C4 plants (Feller et al., 2008a,b). Moreover, RuBisCO amount is modulated by certain genes, which makes a balance between its synthesis and degradation (Sheen, 1990; Krapp et al., 1993), stability of mRNA, polypeptide synthesis, posttranslational modification, assembly of subunits into an active holoenzyme, inhibitors, and other factors that regulate protein degradation (Mehta et al., 1992; Eckardt and Pell, 1995; Desimone et al., 1996; Parry et al., 2008). Impaired regeneration of RuBisCO is an important step in photosynthetic plants, and it results in decreased photosynthetic capacity.

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Tezara et al. (2002) estimated RuBisCO per unit leaf area in sunflower (Helianthus annuus L.) leaves at very mild stress and found that the RuBisCO remained approximately constant, whereas RuBP content rigorously decreased. At severe stress, the decreased activity of RuBisCO was reported, which was dependent on the photosynthetic assimilation of CO2 (A). Apart from this, ribulose bisphosphate content in leaves gets affected and decreases in drought conditions correlating with reduced CO2 assimilation. However, the activity of RuBisCO is not much affected by water stress conditions (Tezara et al., 1999). In point of fact, the activity of RuBisCO under drought condition varies with different plant species and different studies on various crops have yielded different responses of RuBisCO to drought stress. In sunflower and tobacco the effect of drought was very less or nil (Gime´nez et al., 1992; Gunasekera and Berkowitz, 1993; Pankovic et al., 1999; Pelloux et al., 2001). Furthermore, in the C4 grasses, Paspalum dilatatum, Cynodon dactylon, and Zoysia japonica activity of RuBisCO remained unchanged; however, due to the presence or the increase in quantity of an inhibitor such as 2-carboxyarabinitol-1-phosphate (CA1P) under drought stress, RuBisCO activity slightly decreases (Carmo-Silva et al., 2010). Similarly, in tobacco, the decrease in the activity of RuBisCO in drought stress has been reported due to the presence of CA1P inhibitor (Parry et al., 2002). Results from different experiments on soybean (Majumdar et al., 1991), tomato (Bartholomew et al., 1991), Arabidopsis, (Williams et al., 1994), and rice (Zhou et al., 2007) have shown the downregulation of RuBisCO and other associated genes of photosynthesis in response to drought stress treatments. In rice, the drought stress downregulated the expression of chlorophyll a/b-binding protein CP24, PSI reaction center (RC) subunit V, protochlorophyllide reductase A, peptidyl prolyl cis trans isomerase, and other associated proteins (Wang et al., 2011). Similarly, the study on physic nut (Jatropha curcas L.) yielded the downregulation of PSI, PSII, light-harvesting complex proteins, and gene encoding key enzymes in the Calvin cycle, Rubisco small subunit (RbcS), PGK and PRK (Zhang et al., 2015a,b). Furthermore, in sunflower and wheat, the increase of severity and time of exposure to drought stress resulted in the decrease in activity and amount of RuBisCO (Kicheva et al., 1994; Tezara and Lawlor, 1995; Flexas et al., 2006). If the plant is exposed to severe drought for a prolonged duration, permanent cell death will occur, which cannot revive on rewatering. Moreover, there is a synchronized modulation in the expression of enzymes, for example, drought stress decreases the level of RbcS transcript and turns on the expression of cytosolic glutamine synthetase (Bauer et al., 1997). According to Galme´s et al. (2010), under water limiting conditions in 11 of the Mediterranean species with low chloroplastic CO2 concentration (Cc), the deactivation of RuBisCO sites occurs; however, the onset of Cc causing deactivation of RuBisCO also depends upon the leaf characteristics. Plant species acclimatize themselves to severe drought condition by adapting to functioning at low Cc and the amount of ATP generation gets slowed down due to the decrease in the activity or loss of ATP synthase (Pinheiro and Chaves, 2011). Furthermore, Jedmowski et al. (2014) observed the effect of drought on photosynthetic capacity of eight Eurasian and North African genotypes of wild barley (Hordeum spontaneum) and found different photosynthetic responses for drought like in HOR10164, stomatal closure mainly decreased the photosynthetic rate and drought upregulated the expression of the NADP-malate dehydrogenase to initiate malate-OAA shuttle that protects from oxidative damage. However, in HOR10710, the decreased number of QA-reducing

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RCs and the reduced activity and content of RuBisCO negatively affected the photosynthetic rate. Similarly, in Phaseolus vulgaris, the impact of drought on the photosynthetic efficiency was studied (Dias and Bru¨ggemann, 2010); these authors found a decrease in photosynthesis under drought due to reduced intercellular CO2 concentration, decline in the photochemical Chl fluorescence quenching, quantum yield of PSII, and electron transport rate that generated higher pH gradient and more heat dissipation. Apart from this, the Calvin cycle enzymes such as RuBisCO, SFBPase, and Ru5PK were also estimated under drought conditions (Dias and Bru¨ggemann, 2010). Moreover, activities of other enyzmes such as phosphoenolpyruvate (PEP) carboxylase, nicotinamide adenine dinucleotide phosphatemalic enzyme, fructose-1,6-bisphosphatase, and pyruvate orthophosphate dikinase also get affected and decrease with lowering of water content in plants (Farooq et al., 2009). However, the sensitivity toward water stress is more in pyruvate orthophosphate dikinase than other enzymes participating in photosynthesis process (Du et al., 1996). Apart from abovementioned enzymes, reduction in activities of UDP-glucose pyrophosphorylase 2,3-bisphosphoglycerate independent phosphoglycerate mutase and S-adenosylmethionine synthetase was also found in soybean root under drought conditions (Alam et al., 2010). Flooding of water also causes a stress to the plant by generating hypoxic condition. This verity of stress is determined by the depth of the water column, the duration of the flooded condition, and also on-plant genetic traits (Colmer and Voesenek, 2009). Water logging creates an anaerobic situation as the water displaces the O2 attached to the pores of soil. As a result, plants experience O2-deficient stress and thus reduce oxidative phosphorylation and ATP levels. Waterlogging decreases water absorption in root that causes leaf dehydration as a result wilting occurs in plants. Moreover, waterlogging also reduces stomatal conductance (gs) due to less root permeability and low root hydraulic conductivity (Tournaire-Roux et al., 2003; Aroca et al., 2011). There are varied levels of response among the citrus genotypes; for gas exchange parameters under flooded conditions, for instance, the sensitive genotypes show reduction in CO2 assimilation rate and carboxylative efficiency, whereas the tolerant genotype maintains it for long (Hossain et al., 2009). Stomata get close in response alteration in hormone secretion due to the decrease in absorption of water by roots. Furthermore, the closure of stomatal pores reduces the intercellular CO2 concentration, Ci, and the photosynthetic rate (PN) (Herrera, 2013). According to Mutava et al. (2015), there are many factors that contribute to decrease in net photosynthesis under drought and flooding. Moreover, these authors used four contrasting soybean genotypes for tolerance or susceptibility to flooding and drought. It has been reported that the accumulation of starch granules regulates the reduction of net photosynthesis under flood stress. Moreover, ferritin protein plays a major role under flood conditions by protecting plant cells from oxidative damage (Kamal et al., 2015). Along with oxygen, the absorption of nitrogen and other nutrients also becomes limited, which affects the content and/or activity of RuBisCO, hence inhibiting photosynthesis. Moreover, downregulation of PSII light complex has been found, which, in turn, affects the overall growth of plants (Herrera, 2013). Plants adapt to flooding conditions by synthesis of new aquaporins, which will restore the RuBisCO activity, chlorophyll contents, and PN. However, plants that remain in submerged conditions have sufficient plasticity to grow in aquatic environments, such as development of aerenchyma tissue in the root cortex and adventitious root

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formation, reduce the number of root hairs per unit of root length and elongation of submerged internodes (Vasellati et al., 2001; Iglesias-Ferna´ndez and Matilla, 2016). In contrast to drought conditions, stomatal closures occur in response to ethylene (ET)-triggered gene expression. It has been observed in the leaves of flooded strawberry plants that the stomatal closure occurs due to ethylene in spite of ABA delivery through the roots in the xylem and transports to the leaves having strongly depressed (Blanke and Cooke, 2004; IglesiasFerna´ndez and Matilla, 2016). Fig. 27.4 represents the events happening in plants under drought stress.

27.2.2 Salt stress In the environment, salt stress is one of the most important abiotic stresses, placing a severe constraint on growth and yield of crops globally (Parida and Das, 2005; Purty et al., 2008; Kumari et al., 2009; Hoang et al., 2016; Joshi et al., 2016a,b). Hoang et al. (2016) FIGURE 27.4 Proposed scheme represents the event happening in plant under drought stress. Source: Modified from Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S.M.A., 2009. Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29, 185 212.

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reported that worldwide, salinity caused the loss of more than 830 million hectares of arable land. It usually occurs due to scarcity of rain, high evaporation from the soil, industrial emissions, deforestation, and excessive use of fertilizers (Munns and Tester, 2008; Haa et al., 2014). These damages often include dehydration, osmotic imbalance, nutrient imbalance, ion toxicity, and cause oxidative stress that results in cellular damage, reduction in growth, and even plant death (Arshi et al., 2010a,b, 2012; Kosova et al., 2011; Qureshi et al., 2013; Zhang et al., 2016), but the Calvin cycle is one of the major targets of salinity toxicity in plants (Biswal et al., 2011). Plants generally respond to salt stress by downregulating photosynthesis, which includes the Calvin cycle as the final step (Brugnoli and Lauteri, 1991; Sudhir and Murthy, 2004; Munns et al., 2006; Arfan et al., 2007; Chaves et al., 2009; Shu et al., 2013; Tripathi et al., 2016; Joshi et al., 2017; Gupta et al., 2017). It has been reported that salinity resulted in the reduction of photosynthesis via stomatal limitation (Bota et al., 2004; Li et al., 2007) and nonstomatal limitations, including stomatal closure, loss of photosynthetic pigment, reduction of RuBisCO activity, inhibition of carbon assimilation, and degradation of membrane proteins in the photosynthetic apparatus (Mittal et al., 2012; Gil et al., 2013). Recently, Ben et al. (2018) showed that salt stress along with water stress resulted in growth reduction that was associated with a decline in all photosynthetic parameters, namely, the integrity of PSII, leaf nitrogen content, photosynthetic apparatus proteins, and nitrogen metabolism along with the Calvin Benson cycle in olive. Salt stress depresses the expression of photosystem relevant proteins and chloroplast biosynthesis along with the Calvin cycle in Leymus chinensis (Li et al., 2017). RuBisCO is responsible for the fixation of CO2 in photosynthesis (Mauser et al., 2001). Previous studies have showed that one of the major biochemical limitations, including salt-induced decline in photosynthesis, was the decrease in activity and content of RuBisCO (Ziska et al., 1990; Parry et al., 2002; James et al., 2006). A significantly higher decrease in activity and content of RuBisCO was found in salt-stressed spinach (Delfine et al., 1998, 1999; Wang and Nii, 2000). Stomatal closure was reported as a common cause of decrease in intracellular CO2 concentration and the fixation of CO2, resulting in the reduced activity of RuBisCO and the inhibition of photosynthesis in salt-stressed plants (Bota et al., 2004). It has been reported that under moderate concentration of NaCl in the soil, imposed osmotic effects are caused by decreasing stomatal conductance (gs) and mesophyll conductance (gm), which affects leaf CO2 diffusion, causing a decarbamylation of catalytic sites, thus potentially decreasing RuBisCO activation (Flexas et al., 2004). Later, Lu et al. (2009) found that due to decline in content of large subunit (LSU) of RuBisCO, the low efficiency of carboxylation and lesser activity of RuBisCO was observed in salt-sensitive soybean. He et al. (2014) presented a new sight that under salt stress, the excess formation of chloroplast protrusions (CPs)- and RuBisCO-containing bodies (RCBs) aggravates the degradation of RuBisCO, which results in severe reduction in photosynthesis and in the total activity of RuBisCO in Melrose leaves. However, an upregulation in expression of RuBisCO subunits was reported in rice and tobacco (Kim et al., 2005; Razavizadeh et al., 2009) under salt stress suggesting that the increase in RuBisCO occurs when CO2 efflux is reduced under salt stress, resulting in increased photorespiration (Sobhanian et al., 2011).

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Another key enzyme of the Calvin cycle is SBPase, the role of which is in the regenerative stage of the cycle. It is significant because it acts where carbon acquirement is committed to the regeneration of RuBP, an acceptor molecule. It has been reported that photosynthesis is susceptible to small reductions at SBPase levels (Harrison et al., 1997; Raines et al., 2000). Later, this hypothesis was exploited to design transgenic rice cultivar, and studies revealed that overexpression of SBPase was a successful approach for increasing the salt tolerance in rice; by providing more regeneration of RuBP in the soluble stroma as SBPase is capable of maintaining the RuBisCO activation and preventing the sequestration of RuBisCO activase to the thylakoid membrane from the soluble stroma (Feng et al., 2007). Similarly, it has been recommended that increased expression of another Calvin cycle protein, FBPase activity, takes part in the acclimation of rice seedlings to anaerobic conditions produced by oxidative stress produced in saline conditions (Abbasi and Komatsu, 2004). A brief account of effect of salt stress on plants is depicted in Fig. 27.5.

27.2.3 Temperature stress 27.2.3.1 High temperature Presently, the burden of abiotic stresses on plants is likely to increase due to climatic changes, and among all the abiotic stresses, heat stress is a major factor that affects plant growth, development, and production in many regions around the globe (Semenov and Halford, 2009). Weis (1981) reported that control and heat-treated groups were compared with steady-state patterns of C14-labeled Calvin cycle intermediates, which shows a large decrease in the phosphoglyceroacid/triose phosphate ratio and large increase in the RuBP/phosphoglyceroacid ratio in heat-treated group. In a heat-tolerant rice cultivar FIGURE 27.5 Schematic representations of effect of salt stress, its consequences on the Calvin cycle and plant development.

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(Oryza meridionalis) various protein components of the Calvin cycle including PRK, and RuBP increased consistently in expression under heat stress (Lee et al., 2007). In another study it is shown that some proteins namely chaperonin (Cpn60), heat shock protein 90 (HSP90), heat shock protein 70 (HSP70), and thiamine biosynthesis protein (THI1) have a vindicatory role against stress which increased in leaves through heat stress (Scafaro et al., 2010). These authors indicated that when O. meridionalis was treated with heat, it results in an upregulation of the Calvin cycle (Scafaro et al., 2010). However, this would postulate continuous energy output from electron transport to supply the substrates in need for the reduction stage of the Calvin cycle (Scafaro et al., 2010). Notwithstanding O. meridionalis had enhanced a plenty of enzymes in the Calvin cycle at such a severe temperature while electron transport inhibiting it would prevent both the light and dark reactions of photosynthesis. This could elucidate the considerable decrease in the photosynthetic rate after a heat exposure in O. meridionalis and Oryza sativa. Another study by Scafaro et al. (2010) hypothesized that an increased α to β isoform ratio with heat in rice RuBisCO activase (RCA) is probably a mechanism to regulate the Calvin cycle in response to redox changes related to photosystem damage, rather than being purely a mechanism to enhance RCA activity at high temperature. The speculation that redox regulation of the C-terminal cysteine residues in the α isoform may shift the heat stability of the enzyme should be discovered. In addition, various enzymes associated with the regeneration of RuBP were widely reduced under heat stress, for example, GAPDH A/B subunits in Agrostis stolonifera and Astrostole scabra, PRK in O. sativa, Miscanthus sinensis, A. stolonifera, and A. scabra, SBPase in Glycine max and M. sinensis as well as FBA in G. max and M. sinensis (Ahsan et al., 2010a,b; Sharmin et al., 2013; Lee et al., 2007; Wang et al., 2015). These enzymes play vital roles in carbon flux in the Calvin cycle, determining a photosynthesis rate and carbon assimilation (Rokka et al., 2001). In heat stressed Zea mays, its protein abundance did not get affected or changed while the phosphorylation level of PEP carboxykinase (PEPCK) was decreased (Hu et al., 2015). The PEPCK taking part in C4 photosynthesis catalyzes the release of CO2 from oxaloacetate for the Calvin cycle. Hasanuzzaman et al. (2013) found that the synthesis of starch and sucrose, soluble proteins, large and small subunits of RuBisCO proteins reduces by the heat stress. These authors also reported that heat stress reduced the activities of enzymes such as invertase, ADP-glucose pyrophosphorylase, and sucrose phosphate synthase. A remarkable increase was observed in the expression of transcripts associated with photosynthesis and the encoding polypeptides related to PSII, RuBisCO activase, subunits of RuBisCO, ferredoxins, and enzymes of the Calvin cycle by gene ontology analysis in Solanum tuberosum under moderately elevated temperatures (30 C) (Hancock et al., 2014). 27.2.3.2 Low temperature Temperature is an important abiotic factor that regulates plant functions throughout its growth and development (Penfield, 2008). Cold stress is one of the most common abiotic stresses that negatively affects the growth and production of plants resulting in substantial economic losses (Zhu et al., 2007; Zeng et al., 2008; Li et al., 2011; Shi et al., 2015). It is classified as chilling (0 C to approximately 15 C) and freezing (,0 C) stress. Low temperature impairs plant growth and development by affecting its basic physiological and biochemical processes, such as photosynthesis, respiration, nutrient absorption, and transport

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(Xin and Browse, 2000; Suzuki et al., 2008) which reduces its productivity (Yan et al., 2006; Ruelland et al., 2009; Heidarvand and Maali-Amiri, 2010; Miura and Furumoto, 2013). The machinery of photosynthesis is found to be most susceptible to cold stress. It has been reported that the main organelle affected by cold stress is chloroplast (Kimball and Salisbury, 1973), thus adversely affecting photosynthesis (Kratsch and Wise, 2000; Ruelland et al., 2009; Biswal et al., 2011; Theocharis et al., 2012; Su et al., 2015). A decrease was observed in chlorophyll content and photosynthetic rates in sugarcane under cold stress (Du et al., 1999; Zhang et al., 2015a,b). Alteration in pigment complexes, reduced photosynthetic rates, destroyed chloroplast structures, restricted electron transport, and reduced enzyme activities were also documented (Marian et al., 2004; Renaut et al., 2005; Lu et al., 2013). Downregulation of RuBisCO and other enzymes of the Calvin cycle were observed because of the plastid degradation due to chilling injury (Fernandez-Garcia et al., 2012). It has also been documented that low temperature results in the accumulation of ROS, as cold disrupts electron transport chain in chloroplasts and mitochondria, which disturbs photosynthesis (Allen and Ort, 2001; Fan et al., 2015) that disturbs the Calvin cycle by affecting its key enzymes, such as inactivating SBPase (Ding et al., 2017) and accelerating degradation of RuBisCO (Yan et al., 2006; Gai et al., 2008). Under cold stress, the proteome was studied in a chilling-tolerant plant of Thellungiella halophyila, and it was reported that approximately 28% of the regulated proteins were associated with photosynthesis (Gao et al., 2009). The regulated proteins were precursors of chloroplast, RbCs and RuBisCO LSUs, glyceraldehydes-3-phosphate dehydrogenase B, precursor of plastocyanin, and chloroplast carbonic anhydrase; oxygen-evolving enhancer, iron sulfur subunit of cytochrome b 6/f complex, and alanine-2-oxoglutarate aminotransferase. These authors concluded that chilling tolerance of T. halophilais was attained by the regulation of chloroplast function. With the aim to improve cold stress tolerance, Ding et al. (2016) used transgenic tomato plants with increased SBPase activities and results showed higher chilling tolerance as electrolyte leakage reduced whereas photosynthetic capacity, regeneration rate of RuBP, and PSII quantum efficiency were increased and led to growth promotion.

27.2.4 Heavy metal stress Stress due to natural and/or anthropogenic activities, a wide range of elements are available in the environment affecting the growth and photosynthesis of plants. According to 2007 CERCLA Priority List of Hazardous Substances (CERCLA, 2007), certain metals have been ranked as per their toxicity effects such as arsenic (ranked first), lead (ranked second), mercury (ranked third), cadmium (ranked seventh), and chromium (ranked 17th) (Chatterjee et al., 2013). Complex proteolytic processes involving plastidial and vacuolar plant proteases maintain the homeostasis between synthesis and degradation of protein such as RuBisCO via the ubiquitin pathway (Feller et al., 2008a,b). Environmental conditions also influence the proteases to act through ATP-dependent and ATP-independent proteolytic pathways (Sakamoto, 2006). Iron (Fe), manganese (Mn), zinc (Zn), and copper (Cu) are essential elements regulating vital cellular processes, including biochemical activities of chlorophyll and photosynthesis in plants (Bashir et al., 2016). Strongly regulated

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storage and distribution of these elements maintains the optimal metabolic rate in plants. However, variation in elemental uptake, distribution, and/or storage equilibrium, especially in chloroplast, can affect cellular metabolism and overall plant development significantly (Bashir et al., 2016). Fe is one of the most important metals. It is evident that Fe storage in ferritin protein and ferric chelate reductase oxidase7 (FRO7 that reduces ferric ion to Fe21), mainly localized in chloroplasts, has a vital role in carbon assimilation and plant development (Lo´pez-Milla´n et al., 2016; Bashir et al., 2016). Another important Fe transporter in chloroplast is permease in chloroplasts 1 (PIC1), the expression pattern of which triggered by Fe toxicity or deficiency notably modifies the development of chloroplast (Lo´pez-Milla´n et al., 2016; Bashir et al., 2016). Similarly, trace levels of manganese (Mn) are required by plants for its survival (vital cofactor in oxygen metabolism), maintaining photosynthesis reaction and disposal of superoxide radicals (Alejandro et al., 2017). Intracellular distribution of Mn is facilitated by resident protein of the trans-golgi network NRAMP2 (NRAMP family of divalent metal transporters), where knockdown alleles of NRAMP2 exhibited a reduced activity of PSII and augmented oxidative stress during Mn-deficient conditions (Alejandro et al., 2017). Likewise, Cu1 transport during photosynthesis is intervened by chloroplast-envelope PIB-type ATPase, called HMA6 (also known as PAA1); again, similar proteins such as HMA1 and HMA8 (PAA2) are also reported to transport Cu in chloroplast (Aguirre and Pilon, 2016; Bashir et al., 2016). Zn cofactor for several enzymes involved in various metabolic activities of a plant is an essential micronutrient, comprising around 10% of protein binding sites (Mustafa and Komatsu, 2016). Another important aspect is Zn transportation, where many zinc-finger proteins are involved with growth and development of plants. For example, B-box (BBX) protein variant BBX21 is linked to light and ABA signaling. Crocco et al. (2018) recently reported that heterologous expression of Arabidopsis thaliana BBX21 (AtBBX21) in potato (S. tuberosum) var. Spunta resulted in higher rates of photosynthesis with a considerable amplification to photosynthetic gene expression, higher stomatal conductance, and increased dimension of the stomatal opening. However, higher quantity of any metal(s) in plants is toxic causing nonspecific inhibition of photosynthesis by affecting metabolism and carbon sequestration mechanism through a number of direct and indirect means. However, higher concentration of Zn is toxic to plants, as it can substitute both iron (Fe) and magnesium (Mg) interfering cellular processes (Marschner, 1995). Van Assche and Clijsters (1990) reported that RuBisCO, PSII activities in P. vulgaris, was suppressed due to Zn toxicity that was competing with and replacing Mg from RuBisCO. Proteomic studies on shoots of A. thaliana revealed that protein profiles were distinctly changed in reaction to Zn toxicity (Barkla et al., 2014; Zargar et al., 2015). Again, Cu is toxic in plants in higher concentration, thus being able to generate ROS by catalyzing Haber Weiss and Fenton reactions (Bona et al., 2007). Photosynthetic enzymes and leaf chlorophyll content are greatly affected by Cu toxicity, leading to reduce carbon assimilation and growth inhibition (Adrees et al., 2015). Cu toxicity affects the ubiquitin proteasome pathway and leucine/proline aminopeptidases that in turn reduce the rate of removal of oxidatively damaged proteins (Mustafa and Komatsu, 2016). Shoot development of Portulaca oleracea was halted completely when treated with selenium (Se) or mercury (Hg) (Mustafa and Komatsu, 2016; Maleki et al., 2017). Furthermore, it was reported that unavailability of adequate sulfur (S) created stress under

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S deficiency conditions, where contents of photosynthetic pigments and soluble proteins declined markedly (Bagheri et al., 2017). Arsenic (As) is a nonessential and usually toxic element in plants. When exposed to As, the growth of roots becomes extensively hindered. Again, translocation of this metalloid to shoots and leaves interferes with plants’ physiology and biomass accumulation (Finnegan and Chen, 2012; Mitra et al., 2017). As toxicity leads to damage in cellular membranes, causing electrolyte leakage, oxidative stress, lipid peroxidation, and malondialdehyde production, anthocyanin accumulation in leaves, reduction in transpiration intensity, etc. (Finnegan and Chen, 2012; Gupta and Chatterjee, 2017). However, assessing actual damage to plant metabolism upon exposure to As may vary considerably among different plant species, its size, nutritional status, and growth conditions of the plant at the time of As assimilation. Wang et al. (2012) reported transient effects on parameters such as quantum yield, RuBisCO activity, and chloroplast ATPase activity, when different plants (including hyperaccumulator and nonhyper accumulator) were subjected to As stress. During AsV exposures, a plant strengthens its immune response for continuing its carbon metabolism by stimulating the accumulation of ascorbate that in turn reduces the damage of ROS (Khan et al., 2009). The data on transcriptional profiles and proteomic studies is yet to explain the intricacies and changes on primary carbon metabolism as effects of As; however, studies on nonhyperaccumulating plants such as maize and rice have shown few alterations in the protein richness involved in glycolysis and TCA cycle (Chakrabarty et al., 2009; Ahsan et al., 2010a,b; Finnegan and Chen, 2012). Several reports suggest that AsV, AsIII, and MMAIII applications affect net photosynthesis from carbon input into metabolism level, where a decrease in chlorophyll content affects the light harvest capacity and PSII activity in plants (Stoeva and Bineva, 2003; Duman et al., 2010; Finnegan and Chen, 2012; Chatterjee et al., 2017). The decrease in the electron flow through the membranes of thylakoid occurs due to As and subsequently reduces the production potential of ATP and NADPH, which are necessary for carrying out the carbon fixation reactions. Ahsan et al. (2010a,b) reported that in rice leaves, AsV treatment reduces the content of LSUs of RuBisCO, which is determined by the plastid DNA. However, Abercrombie et al. (2008) reported the enhancement in RbCs transcripts in AsV-treated Arabidopsis. Thus it is evident that As not only interferes with carbon fixation capacity but also affects chloroplast DNA gene expression (Finnegan and Chen, 2012). Reductive PPP is associated with enzyme activities triggered by stimulation of light; however, AsIII is reported to inhibit photosynthetic CO2 fixation by reducing the available amount of carbon (Marques and Anderson, 1986). Furthermore, AsIII can bind to a range of thiol-containing proteins (targeting dithiol group of dihydrolipoamide) and cofactors such as mtPDC (mitochondrial pyruvate dehydrogenase complexes), ptPDC (plastid pyruvate dehydrogenase complexes), GDC (glycine decarboxylase complex), OGDC (2-oxoglutarate dehydrogenase complex), and BCOADC (branched-chain 2-oxoacid decarboxylase complex) (Bergquist et al., 2009). The enzyme lipoamide dehydrogenase (LPD) that is present in the lipoamide-containing complexes catalyzes the allocation of electrons to NAD1 from the reduced dihydrolipoamide cofactor; the enzyme gets inactivated by AsIII (not by AsV) through binding to AsIII-specific conserved dithiol existing in LPD (Chen et al., 2010). Ahsan et al. (2010a,b) also demonstrated that LPD is a vital target for As toxicity in Arabidopsis (decreased levels of mtLPD, knockout lines) compared to their wild type counterparts as

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hyperaccumulator Pteris vittata was reported to adapt to As toxicity by reducing carbon metabolism in leaves by significantly declining the associated proteins such as chloroplast and mitochondrial F1Fo ATP synthase, RbCs and RuBisCO LSUs, seduheptulose-1,7bisphosphatase, pyruvate dehydrogenase, malate dehydrogenase, triose-phosphate isomerase, etc. (Bona et al., 2010; Finnegan and Chen, 2012). Marmiroli et al. (2014) reported that AsIII and AsV toxicities were more pronounced in the absence of silica (Si) supplementation in tomato plants. However, the application of Fe and (Si) materials considerably reduces the arsenic toxicity by lowering its concentration in plant parts especially in leaves and hence prevents photosynthetic apparatus from further damage (Sanglard et al., 2016; Bakhat et al., 2017; Mitra et al., 2017). Lead (Pb) toxicity is manifested by the inhibition of photosynthesis. Pb interferes with key photosynthetic enzymes such as ferredoxin NADP1 reductase and deltaaminolevulinic acid dehydratase (ALAD) by reducing their activities, which is further manifested by distorted chloroplast ultrastructure through distorted protein conformation (Pourrut et al., 2011). Several authors have reported inhibition of enzymatic catalysis in Calvin cycle, reduced carotenoid and plastoquinone synthesis, impaired uptake and substitution of essential elements, decreased carbon dioxide assimilation, etc. (Cenkci et al., 2010; Pourrut et al., 2011). Reports suggested that chlorophyll b is more susceptible than chlorophyll a to Pb exposure, which are broken down into phytol, and other products (of the porphyrin ring) by activated enzymes such as chlorophyllase, pheophorbide a oxygenase, Mg-dechelatase (Xiong et al., 2006; Pourrut et al., 2011). Due to the loss of pigment content due to Pb toxicity, photosynthesis is badly affected. Mercury (Hg) is one of the most toxic metals without any known biological function in plants. When accumulated in plants, it causes significant reduction in leaf area, net photosynthesis, and plant growth. The RC proteins even of photosynthetic bacteria (Rhodobacter sphaeroides) get impaired due to Hg contamination (Sipka et al., 2017). Beauvais-Flu¨ck et al. (2017) reported cellular toxicity pathways with dysregulated energy metabolism and transport in Chlamydomonas reinhardtii when exposed to both inorganic-Hg (IHg) and methylHg (MeHg). However, it was evident that MeHg was affecting more to perturb cell’s functions as the bioavailability of MeHg was found to be manyfold (up to 27 3 in C. reinhardtii) higher than for IHg (Beauvais-Flu¨ck et al., 2017). Similar findings were also reported in Hg exposed duckweed Lemna minor, with a considerable decline in photosynthetic pigments and increase in malondialdehyde and lipoxygenase activities (Zhang et al., 2017). Cadmium (Cd), the lethal heavy metal with lesser known biological function, is comparatively a rare element in the Earth crust (To´th et al., 2012). Anthropogenic activities such as mining, metal, and fertilizers production contribute towards the addition of Cd in the terrestrial environment. Having comparatively long biological halftime, Cd21 is usually accumulated within plants and can affect various physiological activities, including photosynthesis (To´th et al., 2012). Cd21 reacts and/or replaces the metal cations (Zn21, Cu21, Ca21) that are present as active groups in metalloproteins. Enzymes involved in photosynthesis such as ribulose-5-phosphate kinase, GADPH, fructose-1,6-bisphosphatase are affected by Cd21. Reports suggest that both the donor and the acceptor components of PSII, FNR, PSI acceptor side suffer damages upon in vitro exposure to Cd21 (Grzyb et al., 2004; Faller et al., 2005). Cd reaches chloroplasts through the xylem after being absorbed by the root system. Again, secondary effects influence the photosynthetic machinery in

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chloroplasts as metal homeostasis is disturbed due to abnormality in the metal transport such as iron deficiency (To´th et al., 2012). Considerable reduction in PSII activity and plant growth with an associated rise in proline levels in Brassica juncea (Indian mustard) was evident upon Cd exposure in a concentration-dependent manner (Sharmila et al., 2017). Cd21 hampers the slow phase of the light-induced oxidation kinetics of P700, which is associated with the Calvin Benson cycle. As Cd21 can interact with the free thiol ( SH) group present in the enzymes involved with the CO2 fixing mechanism such as RuBisCO, the decrease in substrate level enzyme activity is also evident (Siedlecka et al., 1997). Furthermore, in aquatic photosynthetic organisms, CO2 concentrating mechanism (CCM) is required for carboxylation processes in the microenvironment of RuBisCO, which are also affected by Cd21 (To´th et al., 2012). Researchers also demonstrated that Cd exposure to Monochoria hastata plants leads to several visual toxicity symptoms, including chlorosis, withering, and falling of leaves (Baruah et al., 2017; Maleki et al., 2017). Chromium (Cr), primarily occurring as chromite (CrIII) and chromate (CrVI), is a toxic heavy metal that does not have any essential metabolic function in plants. Photosynthesis, nutrient uptake, and plant growth are notably affected by Cr through induction of phytotoxicity by generating more ROS that causes lipid peroxidation and alteration of antioxidant activities (Shahid et al., 2017). CrVI stress leads to enhanced production of hydrogen peroxide, superoxide radical, lipid peroxidation, and membrane damage, in one hand, and to enhanced adenosine triphosphate sulfurylase (ATPS), o-acetylserine(thiol)lyase (OASTL), glutathione reductase (GR), ascorbate peroxidase (APX), and glutathione-Stransferase (GST) activity, on the other (Singh et al., 2017). It was further pointed out that high sulfur augmentation reduces the extent of CrVI and turns on the mechanism that have damaging effects in Solanum melongena seedlings, where glutathione and cysteine play a crucial role (Singh et al., 2017).

27.2.5 Ozone stress Globally, ozone (O3) pollution is creating an emerging risk to agronomists as ozone has toxic effects on major crop production (Ainsworth, 2017). O3 is a natural compound present in both the stratospheric and tropospheric layers of the atmosphere; however, the role of ozone in both the layers is different. In the stratosphere, it protects from harmful UV radiation, whereas in troposphere it is one of the most harmful greenhouse gases (Denman et al., 2007; Solomon et al., 2010). Ozone is a photochemical oxidant produced via photochemical reactions between nitrogen oxides, volatile organic compounds (VOCs), and sunlight. Due to anthropogenic activities such as release of gas from motor vehicles, conventional brick-making kilns, ombustion of crude oil, and ozone precursor gases are released (Akhtar et al., 2010; Chakraborty et al., 2015; Brauer et al., 2016). Jhun et al. (2015) reported that in town areas, it is believed that NOx scavenges O3 (Gregg et al., 2003); however, the reactivity among NOx and O3 is based on the concentration of VOC, light, season, and temperature. Ozone stress mainly affects the process of photosynthesis that is a fundamental process in plants; however, the level of damage depends on the different species of plants. A number of plants are sensitive to ozone to a large extent and have an impact on the growth

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and yield of the plant. In the presence of high concentration of ozone, the stomata cells get closed and in turn transpiration and water conductivity in tissues get reduced. Moreover, closure of stomatal cells decrease the diffusion of CO2, hence the photosynthetic efficiency and carbon assimilation slows down, which reduces the plant growth and yield (McAdam et al., 2017). Ozone, being a strong oxidizing agent, also induces various physiological and metabolic changes, including the generation of ROS in cell such as hydrogen peroxide (H2O2) (Heath, 2008; Paoletti et al., 2010; Rı´o Segade et al., 2017; Cassia et al., 2018). To abolish the generated ROS and to prevent from the damage in plants, a large portion of carbon is diverted toward the synthesis of secondary compounds such as flavonoids, phenolic compounds, and lignins (Kangasja¨rvi et al., 1994; Booker and Miller, 1998; Dizengremel, 2001; Kontunen-Soppela et al., 2007; Castagna and Ranieri, 2009) In addition, plants upregulate the expression of antioxidant enzymes (catalase, ascorbate peroxidase, and glutathione peroxidase) (Foyer and Noctor, 2005). Moreover, in response to ozone stress it has also been observed that photosynthetic cells of plants increase the production of VOCs (C6 compounds, isoprene, and monoterpenes) (Loreto et al., 2004; Velikova et al., 2005; Fares et al., 2006; Loreto and Schnitzler, 2010). Economic loss of approximately 14 26 billion US$ has been estimated due to loss of yield and biomass of crops (Ashrafuzzaman et al., 2017). Recently, the effect of ozone at different concentrations was studied in tomato plants and exposure to ozone reduced the fruit number and fruit size; however, flowering rate and fruit setting rate remained unchanged (Thwe et al., 2015). Furthermore, the negative effect of ozone on rice has been demonstrated through supplementation experiments. Exposure to ozone reduced the overall growth of rice plant (height and tillering), stomatal conductance, SPAD value, vegetation index (NDVI), and lipid peroxidation. The grain yield of sensitive variety such as Bangladeshi BR28 was reduced by 37% on exposure to artificial ozone (Ashrafuzzaman et al., 2017). Moreover, a drop of approximately 3.7% in global production of rice and 10% in local rice yields have been reduced due to the increase of ozone, and this drop is expected to increase with the increase in ozone (Ainsworth, 2008; Van Dingenen et al., 2009; Frei, 2015). Recently, ozone-responsive apoplastic protein1 (OsORAP1), a novel protein, was identified in rice, which induced cell death in response to ozone stress (Ueda et al., 2015). Similarly, ozone has shown detrimental effect on growth and yield of soybean. The responsive proteins found were ATP synthase α-subunit, ATP synthase β-subunit, PGK, aldo/ketoreductase, RuBisCO activase, and glutamine synthetase, which affects the fixation of carbon and reduces the soybean yield (Khan et al., 2013). Bussotti et al. (2011) reassessed the photosynthetic parameters affected on exposure to ozone stress through fluorescence transient (FT) and modulated fluorescence (MF) analysis and stated that ozone stress decreases the photosynthetic efficiency and photosynthetic performance in tree species. Other parameters such as lesser density of PSI, ferredoxine, NADP1, and RuBP also decreased in ozone stress that impaired electron transport chain and hence will affect the Calvin cycle. Furthermore, the free electron can also initiate the production of ROS consequently starting the processes of photooxidation (Bussotti et al., 2011). Furthermore, in ozone-treated plants the parameters related to fluorescence such as relative variable fluorescence, heat deexcitation constant, energy deexcitation were reported higher while the maximum yield of photochemistry (Φpo) was lower in treated plants, which shows the reduction of photosynthetic efficiency (Manes et al., 2001).

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A decrease in photosynthesis marks the carbon fixation and assimilation and as a result reduces plant biomass (Nie et al., 1993). Reduced activity and loss of RuBisCO was reported as a contributing factor for the decrease of CO2 absorption in O3-treated leaves; however, the quantum efficiency of PSII remained unaffected in Plantago major (Zheng et al., 2002). The modulation in quantity and the activity of RuBisCO has a marked effect on CO2 assimilation (Pell et al., 1994). Decreased quantity and abundance of mRNA transcript for the RuBisCO LSUs and RbCs have been found on exposure to O3 stress (Pell et al., 1994, 1997; Zheng et al., 2002). In addition, ozone stress has a major influence on the activity and expression of PEP enzyme. The inhibitory role of ozone on PEP has been reviewed by Dizengremel et al. (2012). The PEP serves as a main precursor in following metabolic routes: 1. Mitochondrial respiration: This process involves breakdown of organic acids (mainly pyruvate) and formation of ATP and NADH, and this energy is used for biosynthesis. 2. Methylerythritol 4-phosphate (MEP) pathway: The MEP pathway contributes to plastidial isoprenoid biosynthesis and is initiated by the starting condensation of pyruvate and GAP. MEP pathway supplies compounds having a role in plant defense. 3. Shikimate phenylpropanoid pathway: It forms aromatic amino acids, precursors of phenolic compounds, and monolignols. PEP from glycolysis and erythrose-4-P from either oxidative PPP or the Calvin cycle condense in chloroplast to form shikimic acid. 4. Anaplerotic pathway: This process starts with PEP carboxylase (PEPc) activity and forms intermediates for the Krebs, TCA, and citric acid cycle. During ozone stress, photosynthetic inhibition results in downregulation of PEP that has prime importance in carbon diversion and its allocation in different pathways involved in cellular respiration and anabolic processes. The enhanced ozone exposure results in decreased expression of PEP that in turn hampers and affects defense response of plant system, especially in scavenging ROS (Dizengremel et al., 2012).

27.2.6 UV-B stress On the Earth surface, one of the existing climate-change causes is enhanced by UV-B radiation due to the reduction of stratospheric ozone layers. To reduce the discharge of such compounds that reduce the ozone layer the Montreal Protocol (1987) was established; in spite of this protocol, the removal has not been reversed (Abbasi and Abbasi, 2017; Sharma et al., 2017), and an increase of 0.6% deterioration continues per year (Prado et al., 2012). UV-B radiation induces a large amount of deviations in the metabolism, morphology, physiology, and molecular levels in plants (Mandi, 2016a,b; Jenkins, 2017). Indeed, UV-B radiation can hamper photosynthesis by causing alteration in gene expression and damage to the photosynthetic machinery, generally to PSI and PSII, light-harvesting complex II (LHCII), and the Calvin cycle and its enzymes. RuBisCO is an important enzyme for assimilation of CO2 in C3 cycle of photosynthesis (Furbank and Taylor, 1995; Hollo´sy, 2002). Lorimer (1981) found that the quantity and activity of RuBisCO affect the rate of photosynthesis and biomass accumulation in plants. UV-B radiation causes a decrease in level and appearance of RuBisCO protein

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(Allen et al., 1998). Previous studies explained that in pea, soybean, and cucumber plants, the activity and the amount of RuBisCO were downregulated by an exposure to UV-B radiation (Vu et al., 1984; Caldwell, 1993; Allen et al., 1997; He et al., 1993, 1994). Jordan et al. (1992) have also demonstrated that after UV-B irradiation, the mRNA transcripts were lesser for RuBisCO LSUs and RbCs in pea, which indicates that the decreased activity of RuBisCO plays a major function in UV-induced reduction of photosynthesis. After UV-B exposure in oilseed rape, pea, tomato, and tobacco, the photomodified form of RuBisCO LSU was observed by the appearance of a 66 kDa protein (Wilson et al., 1995). UV-B affects the carboxylation efficiency not only by altering the activity of RuBisCO, but also by lowering the RuBisCO proteins in leaves of pea (Nogues and Baker, 1995). The damage in RuBisCO protein and activity by UV-B exposure has also been linked to the higher production of ROS in the cells (Allen et al., 1998; Kataria et al., 2014). Allen et al. (1998) found that high UV-B irradiance causes inhibition of photosynthetic ability due to lower enzyme activities of the Calvin cycle. Western blot analyses indicated that UV-B irradiation induced a decrease in the SBPase content, however, not in chloroplastic FBPase or PRK content in leaves of oilseed rape (Allen et al., 1998). RuBisCO synthesis was considerably decreased by enhanced UV-B in rice leaves (Takeuchi et al., 2002). Choi and Rho (2003) found that the content of RuBisCO protein was lesser in UV-B-irradiated tissues compared with the untreated control due to UV-B, which inhibits the activation and stimulation of RuBisCO activase content and activity. He et al. (2004) observed that UV-B reduces RuBisCO activity by H2O2 stimulating proteolytic enzymes in mung bean cultivars (Phaseolus raditus), and they have also observed that when H2O2 was scavenged by exogenously added ascorbic acid (AsA), it considerably reduced the UV-B-induced reduction of RuBisCO content, enhancement of H2O2 content, and activity of proteolytic enzymes. Fedina et al. (2010) found UV-B-induced stress response in rice cultivars such as Sasanishiki, Norin 1, and Surjamkhi. In their study they found that Sasanishiki was less sensitive to UV-B than Norin 1 and Surjamkhi and the decrease in photosynthetic efficiency in UV-B sensitive rice cultivar may be because of the decrease in electron transport rate and activation of RuBisCO. Correia et al. (2005) found lesser sensitivity to UV-B radiation in terms of photosynthesis in the N-deprived plants, and it was linked with lower reduction in RuBisCO and PEPCase activity as compared to N-nourished plants. Cechin et al. (2018) also showed that the response of sunflower plants to UV-B radiation is based on the supply of nitrogen. They also observed that under low nitrogen supply the decrease in photosynthesis was moderately related to stomatal limitation, although under high nitrogen supply, photosynthesis was under control of mesophyll metabolism that decreased the demand for CO2; it may be due to the fact that under high nitrogen, the decline in the RuBisCO content or activity might plays an important role in an increase of CO2. The large decreases in the Calvin cycle enzymes such as RuBisCO and SBPase were observed after UV-B exposure in higher plants without any considerable effect on PSII (Nogues et al., 2006). The results of Kataria et al. (2013) demonstrated that solar UV exclusion significantly enhanced the RuBisCO activity in C3 and C4 crop species along with increase in soluble protein content; which indicates that ambient UV-B inhibits the activity of RuBisCO. Bischof et al. (2002) also found the increase in RuBisCO content and activity after the exclusion of solar UV radiation in Ulva lactuca. The active oxygen species formed under UV-B radiation damages RuBisCO proteins (Hideg et al., 2000). Although several studies

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have shown that the reduction in rate of photosynthesis is because of the sensitivity of PSII to UV-B (Bornman, 1989; Melis et al., 1992), the decrease in CO2 absorption by UV-B takes place earlier to or in the absence of despair in PSII and may involve the destruction in the Calvin cycle enzyme RuBisCO (Nogues and Baker, 1995; Allen et al., 1998). Ambient UV-B reduced the photosynthetic performance in arctic plants due to the decrease in the maximum electron rate (Jmax), which results in reduced RuBP regeneration and maximum rate of RuBisCO carboxylation (Vcmax) (Albert et al., 2011). Kataria et al. (2013) also found that the quantum yield of electron transport was reduced under ambient UV radiation in plants, which may be due to the fact that linear flow of electrons further decreased compared to PSII as a consequential lesser quantity of electrons are available for the Calvin cycle. Impaired net rate of CO2 assimilation, photosynthesis, oxidative stress, transpiration rate, photosynthetic pigments, and RuBisCO activity was found when young olive plants (cv. “Galega Vulgar”) were exposed to 5 days of biologically effective doses of 6.5 and 12.4 kJ/m2/day UV-B (Dias et al., 2018).

27.3 Conclusion and future perspectives There have been several evidences that natural abiotic stresses such as drought, salt stress, high and low temperature, ozone, and UV-B inhibit the photosynthesis due to damage in PSII activity and inhibition of the enzymes’ activities of the Calvin cycle (Fig. 27.6). All the FIGURE 27.6 Schematic representations of effect of different abiotic stresses on plants (Calvin cycle) and their responses. Source: Modified from Malhotra, C., Kapoor, R.T., 2019. Silicon: a sustainable tool in abiotic stress tolerance in plants. In: Hasanuzzaman, M., Hakeem, K., Nahar, K., Alharby, H. (Eds.) Plant Abiotic Stress Tolerance. Springer, Cham, Chapter-14, pp. 333 356.

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27. Regulation of the Calvin cycle under abiotic stresses: an overview

above mentioned environmental factors eventually reduce the activity of the Calvin cycle directly or indirectly via stomatal closure in higher plants (Fig. 27.6). Stomatal closure takes part in the reduction of leaf photosynthesis, and RuBisCO is a main enzyme of the Calvin cycle for photosynthetic processes, the deprivation of which is based on the strength of abiotic stresses. Stomatal closure affected photosynthesis by decreasing the availability of CO2 for absorption by RuBisCO and the interruption of the Calvin cycle repressed the repair of the PSII photodamaged under abiotic stress conditions. Thus the vulnerability of the Calvin cycle to ecological stresses may possibly conclude the tolerance of PSII to the stress. Furthermore, in each abiotic stress condition, the ultimate responses of plants is the increase of ROS, such as singlet oxygen, superoxide radicals, hydroxyl radicals, and hydrogen peroxide, which impart oxidative stress by damaging various biomolecules of the cell. Initiation of redox reactions regulates signal transduction, gene expression, protein synthesis, thiol-disulphide exchange reactions, and finally alters metabolism. Moreover, the stress exerts an extra burden on the plant metabolism as combating damaging effects of stress diverts its metabolic energy in biosynthesis and expression of various antioxidants and antioxidant enzymes. This mechanism of counterbalancing the oxidative damage leads either to stress acclimation by compromising in growth and yield of crop or to senescence and cell death based on the extent of the oxidative stress. In addition, sometimes two or more stresses may act over plants simultaneously, which may disturb plant hormonal homeostasis and metabolism. Therefore, there is an urgent need to understand plant regulation under stress and interaction with various factors helping plants under multiple stress conditions, which may further be beneficial to screen the better performing, resistant crops to ensure food security, and agricultural sustainability globally. Preferably, extensive sets of experiments should be carried out with multiple stresses for data generation on physiological changes with the increasing adverse and variable environments. Response to specific stress is highly dependent on the level of tolerance or susceptibility of plants to the abiotic stresses that is predominantly regulated by the appearance of the nuclear genes and proteins. The major challenge for researchers is to enhance the levels of abiotic stress tolerance in plants by increasing the photosynthetic production. Earlier attempts mostly focused on gene expression studies; however, RNA data is inadequate. Further studies in the field of proteomic, transcriptomic, metabolomic changes, and novel cellular imaging techniques would substantially enhance our understanding of photosynthetic machinery under abiotic stresses. In the future perspectives, the various steps in RuBisCO degradation, the proteolytic enzymes involved in these processes remain to be explained under abiotic stress conditions.

Acknowledgments The authors acknowledge Mrs. Deeksha Paliwal for her contribution in helping with diagrams. Financial support by the Department of Science Technology Women Scientists-A Scheme (SR/WOS-A/LS-17/2017) to Dr. Sunita Kataria is thankfully acknowledged.

References Abbasi, S.A., Abbasi, T., 2017. Monitoring ozone loss and its consequences: past, present, and future. In: Abbasi, S.A., Abbasi, T. (Eds.), Ozone Hole. Springer, New York, pp. 121 131.

Plant Life under Changing Environment

References

705

Abbasi, F.M., Komatsu, S., 2004. A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4, 2072 2081. Available from: https://doi.org/10.1002/pmic.200300741. Abercrombie, J.M., Halfhill, M.D., Ranjan, P., Rao, M.R., Saxton, A.M., Yuan, J.S., et al., 2008. Transcriptional responses of Arabidopsis thaliana plants to As (V) stress. BMC Plant Biol. 8, 87. Available from: https://doi. org/10.1186/1471-2229-8-87. Adrees, M., Ali, S., Rizwan, M., Ibrahim, M., Abbas, F., Farid, M., et al., 2015. The effect of excess copper on growth and physiology of important food crops: a review. Environ. Sci. Pollut. Res. Int. 22, 8148 8162. Aguirre, G., Pilon, M., 2016. Copper delivery to chloroplast proteins and its regulation. Front. Plant Sci. 6, 1250. Available from: https://doi.org/10.3389/fpls.2015.01250. Ahmadi, A., Baker, D.A., 2001. The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat. Plant Growth Regul. 35, 81 91. Ahsan, N., Donnart, T., Nouri, M.Z., Komatsu, S., 2010a. Tissue-specific defense and thermo-adaptive mechanisms of soybean seedlings under heat stress revealed by proteomic approach. J. Proteome. Res. 9, 4189 4204. Ahsan, N., Lee, D.G., Kim, K.H., Alam, I., Lee, S.H., Lee, K.W., et al., 2010b. Analysis of arsenic stress-induced differentially expressed proteins in rice leaves by two-dimensional gel electrophoresis coupled with mass spectrometry. Chemosphere 78, 224 231. Ainsworth, E.A., 2008. Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration. Global Change Biol. 14, 1642 1650. Ainsworth, E.A., 2017. Understanding and improving global crop response to ozone pollution. Plant J. 90, 886 897. Akhtar, N., Yamaguchi, M., Inada, H., Hoshino, D., Kondo, T., Fukami, M., et al., 2010. Effects of ozone on growth, yield and leaf gas exchange rates of four Bangladeshi cultivars of rice (Oryza sativa L.). Environ. Pollut. 158, 2970 2975. Ashrafuzzaman, M., Lubna, F.A., Holtkamp, F., Manning, W.J., Kraska, T., Frei, M., 2017. Diagnosing ozone stress and differential tolerance in rice (Oryza sativa L.) with ethylenediurea (EDU). Environ. Pollut. 230, 339 350. Alam, I., Sharmin, S.A., Kim, K.H., Yang, J.K., Choi, M.S., Lee, B.H., 2010. Proteome analysis of soybean roots subjected to short-term drought stress. Plant Soil 333, 491 505. Albert, K.R., Mikkelsen, T.N., Ro -Poulsen, H., Arndal, M.F., Michelsen, A., 2011. Ambient UV-B decreases PS II performance and net photosynthesis in high arctic Salix arctica. Environ. Exp. Bot. 72, 439 447. Alejandro, S., Cailliatte, R., Alcon, C., Dirick, L., Domergue, F., Correia, D., et al., 2017. Intracellular distribution of manganese by the trans-Golgi network transporter NRAMP2 is critical for photosynthesis and cellular redox homeostasis. Plant Cell 29 (12), 3068 3084. Allen, D.J., Mckee, I.F., Farage, P.K., Baker, N.R., 1997. Analysis of limitations to CO2 assimilation on exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ 20, 633 640. Allen, D.J., Ort, D.R., 2001. Impacts of chilling temperatures on photosynthesis in warm climate plants. Trends Plant Sci. 6, 36 42. Allen, D.J., Nougu´es, S., Baker, N.R., 1998. Ozone depletion and increased UV-B radiation: is there a real threat to photosynthesis? J. Exp. Bot. 49, 1775 1778. Antonio, C., Pinheiro, C., Chaves, M.M., Ricardo, C.P., Ortuno, M.F., Thomas-Oates, J., 2008. Analysis of carbohydrates in Lupinusalbus stems on imposition of water deficit, using porous graphitic carbon liquid chromatography-electrospray ionization mass spectrometry. J. Chromatogr. A 1187, 111 118. Arfan, M., Athar, H.R., Ashraf, M., 2007. Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? J. Plant Physiol. 164, 685 694. Aroca, R., Porcel, R., Ruiz-Lozano, J.M., 2011. Regulation of root water uptake under abiotic stress conditions. J. Exp. Bot. 63, 43 57. Arshi, A., Ahmad, A., Aref, I.M., Iqbal, M., 2010a. Calcium interaction with salinity induced effects on growth and metabolism of soybean (Glycine max L.) cultivars. J. Environ. Biol. 31, 795 801. Arshi, A., Ahmad, A., Aref, I.M., Iqbal, M., 2010b. Effect of calcium against salinity-induced inhibition in growth, ion accumulation and proline contents in Cichorium intybus L. J. Environ. Biol. 31, 939 944. Arshi, A., Ahmad, A., Aref, I.M., Iqbal, M., 2012. Comparative studies on antioxidant enzyme action and ion accumulation in soybean cultivars under salinity stress. J. Environ. Biol. 33, 9 20. Bagheri, R., Ahmad, J., Bashir, H., Iqbal, M., Qureshi, M.I., 2017. Changes in Rubisco, cysteine-rich proteins and antioxidant system of spinach (Spinacia oleracea L.) due to sulphur deficiency, cadmium stress and their combination. Protoplasma 254, 1031 1043.

Plant Life under Changing Environment

706

27. Regulation of the Calvin cycle under abiotic stresses: an overview

Bakhat, H.F., Zia, Z., Fahad, S., Abbas, S., Hammad, H.M., Shahzad, A.N., et al., 2017. Arsenic uptake, accumulation and toxicity in rice plants: possible remedies for its detoxification: a review. Environ. Sci. Pollut. Res. 24, 9142 9158. Barkla, B.J., Vera-Estrella, R., Miranda-Vergara, M.C., Pantoja, O., 2014. Quantitative proteomics of heavy metal exposure in Arabidopsis thaliana reveals alterations in onecarbon metabolism enzymes upon exposure to zinc. J. Proteome 111, 128 138. Bartholomew, D.M., Bartley, G.E., Scolnik, P.A., 1991. Abscisic-acid control of rbcS and cab transcription in tomato leaves. Plant Physiol. 96, 291 296. Baruah, S., Bora, M.S., Sharma, P., Deb, P., Sarma, K.P., 2017. Understanding of the distribution, translocation, bioaccumulation, and ultrastructural changes of Monochoria hastata plant exposed to cadmium. Water Air Soil Pollut. 228 (1), 17. Bashir, K., Rasheed, S., Kobayashi, T., Seki, M., Nishizawa, N.K., 2016. Regulating subcellular metal homeostasis: the key to crop improvement. Front. Plant Sci. 7, 1192. Available from: https://doi.org/10.3389/fpls.2016.01192. Basu, S., Ramegowda, V., Kumar, A., Pereira, A., 2016. Plant adaptation to drought stress. F1000Res. 5, F1000 Faculty Rev-1554. Available from: https://doi.org/10.12688/f1000research.7678.1. Bauer, D., Biehler, K., Fock, H., Carrayol, E., Hirel, B., Migge, A., et al., 1997. A role for cytosolic glutamine synthetase in the remobilization of leaf nitrogen during water stress in tomato. Physiol. Planta 99, 241 248. Beauvais-Flu¨ck, R., Slaveykova, V.I., Cosio, C., 2017. Cellular toxicity pathways of inorganic and methyl mercury in the green microalga Chlamydomonas reinhardtii. Sci. Rep. 7 (1), 8034. Available from: https://doi.org/ 10.1038/s41598-017-08515-8. Ben, A.M., Trupiano, D., Polzella, A., De, Z.E., Sassi, M., Scaloni, A., et al., 2018. Unravelling physiological, biochemical and molecular mechanisms involved in olive (Olea europaea L. cv. Che´toui) tolerance to drought and salt stresses. J. Plant Physiol. 220, 83 95. Benson, A.A., Calvin, M., 1950. Carbon dioxide fixation by green plants. Annu. Rev. Plant Physiol. 1, 25 42. Bergquist, E.R., Fischer, R.J., Sugden, K.D., Martin, B.D., 2009. Inhibition by methylated organoarsenicals of the respiratory 2-oxo-acid dehydrogenases. J. Organomet. Chem. 694, 973 980. Bischof, K., Krabs, G., Wiencke, C., Hanelt, D., 2002. Solar ultraviolet radiation affects the activity of ribulose-1,5bisphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta 215, 502 509. Biswal, B., Joshi, P., Raval, M., Biswal, U., 2011. Photosynthesis, a global sensor of environmental stress in green plants: stress signalling and adaptation. Curr. Sci. 101, 47 56. Bjo¨rkman, O., 1981. Response to different quantum flux intensities. In: Lange, O.L., Nobel, P.S., Osmond, C.B., Zeigler, H. (Eds.), Encyclopedia of Plant Physiology, vol. 12. Springer-Verlag, Heidelberg, pp. 57 107. Blanke, M., Cooke, D.T., 2004. Effects of flooding and drought on stomatal activity, transpiration, photosynthesis, water potential and water channel activity in strawberry stolons and leaves. Plant Growth Regul. 42, 153 160. Bona, E., Marsano, F., Cavaletto, M., Berta, G., 2007. Proteomic characterization of copper stress response in Cannabis sativa roots. Proteomics 7, 1121 1130. Bona, E., Cattaneo, C., Cesaro, P., Marsano, F., Lingua, G., Cavaletto, M., et al., 2010. Proteomic analysis of Pterisvittata fronds: two arbuscular mycorrhizal fungi differentially modulate protein expression under arsenic contamination. Proteomics 10, 3811 3834. Bota, J., Flexas, J., Medrano, H., 2004. Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytol. 162, 671 681. Brandes, H.K., Hartmann, F.C., Lu, T.-Y., Larimer, F.W., 1996. Efficient expression of the gene for spinach phosphoribulokinase in Picia pastoris and utilization of the recombinant enzyme to explore the role of regulatory cysteinyl residue by site-directed mutagenesis. J. Biol. Chem. 271, 6490 6496. Brugnoli, E., Lauteri, M., 1991. Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt tolerant (Gossypium hirsutum L.) and salt-sensitive (Phaseolus vulgaris L.) C3 nonhalophytes. Plant Physiol. 95, 628 635. Bryant, B., 2000. The Production and Analysis of Tobacco Plants With Reduced Levels of the Calvin Cycle Enzyme Sedoheptulose-1,7-Bisphosphatase (Ph.D. thesis). University of Essex. von Caemmerer, S., 2000. Biochemical Models of Leaf Photosynthesis. CSIRO Publishing, Collingwood, Australia. Booker, F.L., Miller, J.E., 1998. Phenylpropanoid metabolism and phenolic composition of soybean (Glycine max) leaves following exposure to ozone, J. Exp. Bot., 49. pp. 1191 1202.

Plant Life under Changing Environment

References

707

Brauer, M., Freedman, G., Frostad, J., van Donkelaar, A., Martin, R.V., Dentener, F., et al., 2016. Ambient air pollution exposure estimation for the global burden of disease 2013. Environ. Sci. Technol. 50, 79 88. Bornman, J.F., 1989. Target sites of UV-B radiation in photosynthesis of higher plants. J. Photochem. Photobiol. B 4, 145 158. Bussotti, F., Desotgiu, R., Cascio, C., Pollastrini, M., Gravano, E., Gerosa, G., et al., 2011. Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environ. Exp. Bot. 73, 19 30. Caldwell, C.R., 1993. Ultraviolet-induced photodegradation of cucumber (Cucumis sativus L.) microsomal and soluble protein tryptophanyl residues in vitro. Plant Physiol. 101, 947 953. Carmo-Silva, A.E., Keys, A.J., Andralojc, P.J., Powers, S.J., Arrabac¸a, M.C., Parry, M.A.J., 2010. Rubisco activities, properties, and regulation in three different C4 grasses under drought. J. Exp. Bot. 61 (9), 2355 2366. Cattivelli, L., Rizza, F., Badeck, F.W., Mazzucotelli, E., Mastrangelo, A.M., Francia, E., et al., 2008. Drought tolerance improvement in crop plants: an integrative view from breeding to genomics. Field Crop. Res. 105, 1 14. Cechin, I., Gonzalez, G.C., Corniani, N., Terezinha de, F.F., 2018. The sensitivity of sunflower (Helianthus annuus L.) plants to UV-B radiation is altered by nitrogen status. Cieˆncia Rural, Santa Maria 48, 02. e20170369. ¨ zay, C., Bozdag, A., Terzi, H., 2010. Lead contamination reduces chlorophyll Cenkci, S., Cigerci, I.H., Yildiz, M., O biosynthesis and genomic template stability in Brassica rapa L. Environ. Exp. Bot. 67 (3), 467 473. CERCLA, 2007. Priority list of hazardous substances. ,http://www.atsdr.cdc.gov/spl/supportdocs/appendix-d. pdf.. Chakrabarty, D., Trivedi, P.K., Misra, P., Tiwari, M., Shri, M., Shukla, D., et al., 2009. Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74, 688 702. Chatterjee, S., Datta, S., Mallick, P.H., Mitra, A., Veer, V., Mukhopadhyay, S.K., 2013. Use of wetland plants in bioaccumulation of heavy metals. In: Gupta, D.K. (Ed.), Plant-Based Remediation Processes. Springer-Verlag, Berlin, Heidelberg. Available from: https://doi.org/10.1007/978-3-642-35564-6_7. Chatterjee, S., Sharma, S., Gupta, D.K., 2017. Arsenic and its effect on major crop plants: stationary awareness to paradigm with special reference to rice crop. In: Gupta, D.K., Chatterjee, S. (Eds.), Arsenic Contamination in the Environment: The Issues and Solutions. Springer International Publishing AG (2017), pp. 123 143. Available from: https://doi.org/10.1007/978-3-319-54356-7_6. Chaves, M.M., 1991. Effects of water deficits on carbon assimilation. J. Exp. Bot. 42, 1 16. Chaves, M.M., Flexas, J., Pinheiro, C., 2009. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot.-London 103, 551 560. Chen, W., Chi, Y., Taylor, N.L., Lambers, H., Finnegan, P.M., 2010. Disruption of ptLPD1 or ptLPD2, genes that encode isoforms of the plastidiallipoamide dehydrogenase, confers arsenate hypersensitivity in Arabidopsis. Plant Physiol. 153, 1385 1397. Choi, B.Y., Roh, K.S., 2003. UV-B radiation affects chlorophyll and activation of rubisco by rubisco activase in Canavalia ensiformis L. leaves. J. Plant Biol. 46, 117 121. Colmer, T.D., Voesenek, L.A.C.J., 2009. Flooding tolerance: suites of plant traits in variable environments. Funct. Plant Biol. 36, 665 681. Cornic, G., 2000. Drought stress inhibits photosynthesis by decreasing stomatal aperture not by affecting ATP synthesis. Trends Plant Sci. 5, 187 188. Crocco, C.D., Gomez-Ocampo, G., Mantese, A., Ploschuk, E.L., Botto, J.F., 2018. Heterologous expression of AtBBX21 enhances the rate of photosynthesis and alleviates photoinhibition in Solanum tuberosum. Plant Physiol. 01417.2017. Available from: https://doi.org/10.1104/pp.17.01417. pii. Cassia, R., Nocioni, M., Correa-Aragunde, N., Lamattina, L., 2018. Climate change and the impact of greenhouse gasses: CO2 and NO, friends and foes of plant oxidative stress. Front. Plant Sci. 9, 273. Available from: https://doi.org/10.3389/fpls.2018.00273. Castagna, A., Ranieri, A., 2009. Detoxification and repair process of ozone injury: from O3 uptake to gene expression adjustment. Environ. Pollut. 157, 1461 1469. Chakraborty, T., Beig, G., Dentener, F.J., Wild, O., 2015. Atmospheric transport of ozone between southern and eastern Asia. Sci. Total Environ. 523, 28 39. Delfine, S., Alvino, A., Zacchini, M., Loreto, F., 1998. Consequences of salt stress on conductance to CO2 diffusion, Rubisco characteristics and anatomy of spinach leaves. Aust. J. Plant Physiol. 25, 395 402. Delfine, S., Alvino, A., Villani, M.C., Loreto, F., 1999. Restrictions to CO2 conductance and photosynthesis in spinach leaves recovering from salt stress. Plant Physiol. 119, 1101 1106.

Plant Life under Changing Environment

708

27. Regulation of the Calvin cycle under abiotic stresses: an overview

Desimone, M., Henke, A., Wagner, E., 1996. Oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiol. 111, 789 796. Dias, M.C., Bru¨ggemann, W., 2010. Limitations of photosynthesis in Phaseolus vulgaris under drought stress: gas exchange, chlorophyll fluorescence and Calvin cycle enzymes. Photosynthetica 48, 96. Dias, M.C., Pinto, D.C.G.A., Correiac, C., Moutinho-Pereira, J., Oliveira, H., Freitas, H., et al., 2018. UV-B radiation modulates physiology and lipophilic metabolite profile in Olea europaea. J. Plant Physiol. 222, 39 50. Ding, F., Wang, M., Zhang, S., Ai, X., 2016. Changes in SBPase activity influence photosynthetic capacity, growth, and tolerance to chilling stress in transgenic tomato plants. Sci. Rep. 6, 32741. Ding, F., Wang, M., Zhang, S., 2017. Overexpression of a Calvin cycle enzyme SBPase improves tolerance to chilling-induced oxidative stress in tomato plants. Sci. Hortic. 214, 27 33. Denman, K.L., Brasseur, G., Chidthaisong, A., Ciais, P., Cox, P.M., Dickinson, R.E., et al., 2007. Couplings between changes in the climate system and biogeochemistry. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp. 499 587. De Oliveira, A.B., Mendes Alencar, N.L., Gomes-Filho, E., 2013. Comparison between the water and salt stress effects on plant growth and development. In: Akinci, S. (Ed.), Responses of Organisms to Water Stress. InTech. Dizengremel, P., 2001. Effects of ozone on the carbon metabolism of forest trees. Plant. Physiol. Biochem. 39, 729 742. Dizengremel, P., Vaultier, M.N., Thiec, D.L., Cabane´, M., Bagard, M., Ge´rant, D., et al., 2012. Phosphoenolpyruvate is at the crossroads of leaf metabolic responses to ozone stress. New Phytol. 195, 512 517. Du, Y.C., Kawamitsu, Y., Nose, A., Hiyane, S., Murayama, S., Wasano, K., et al., 1996. Effects of water stress on carbon exchange rate and activities of photosynthetic enzymes in leaves of sugarcane (Saccharum sp.). Aust. J. Plant Physiol. 23, 719 726. Du, Y.C., Nose, A., Wasano, K., 1999. Effects of chilling temperature on photosynthetic rates, photosynthetic enzyme activities and metabolite levels in leaves of three sugarcane species. Plant Cell Environ. 22, 317 324. Duman, F., Ozturk, F., Aydin, Z., 2010. Biological responses of duckweed (Lemna minor L.) exposed to the inorganic arsenic species As(III) and As(V): effects of concentration and duration of exposure. Ecotoxicology 19, 983 993. Eckardt, N., Pell, E., 1995. Oxidative modification of Rubisco from potato foliage in response to ozone. Plant Physiol. Biochem. 33, 273 282. Ellis, R.J., 1979. The most abundant protein in the world. Trends Food Sci. Technol. 4, 241 244. Evans, J.R., 1996. Effects of light and nutrition on photosynthesis. In: Baker, N.R. (Ed.), Photosynthesis and the Environment, vol. 5. Kluwer Academic Publishers, Dordecht, The Netherlands, pp. 281 304. Faller, P., Kienzler, K., Krieger-Liszkay, A., 2005. Mechanism of Cd21 toxicity: Cd21 inhibits photoactivation of photosystem II by competitive binding to the essential Ca21 site. Biochim. Biophys. Acta Bioenerg. 1706, 158 164. Fan, J., Hu, Z., Xie, Y., Chan, Z., Chen, K., Amombo, E., et al., 2015. Alleviation of cold damage to photosystem II and metabolisms by melatonin in Bermudagrass. Front. Plant Sci. 6, 925. Fang, Y., Xiong, L., 2015. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell. Mol. Life Sci. 72, 673 689. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S.M.A., 2009. Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29, 185 212. Fedina, I., Hidema, J., Velitchkova, M., Georgieva, K., Nedeva, D., 2010. UV-B induced stress responses in three rice cultivars. Biologia Plantarum 54 (3), 571 574. Feller, U., Anders, I., Demirevska, K., 2008a. Degradation of Rubisco and other chloroplast proteins under abiotic stress. Gen. Appl. Plant Physiol. 34, 5 18. Feller, U., Anders, I., Mae, T., 2008b. Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J. Exp. Bot. 59 (7), 1615 1624. Feng, L., Han, Y., Liu, G., An, B., Yang, J., Yang, G., et al., 2007. Overexpression of sedoheptulose-1,7-bisphosphatase enhances photosynthesis and growth under salt stress in transgenic rice plants. Funct. Plant Biol. 34, 822 834. Fernandez-Garcia, N., Romojaro, F., Olmos, E., Estrella, E., Bolarin, M.C., Flores, F.B., 2012. Understanding the mechanisms of chilling injury in bell pepper fruits using the proteomic approach. J. Proteomics 75, 5463 5478. Finnegan, P.M., Chen, W., 2012. Arsenic toxicity: the effects on plant metabolism. Front. Physiol. 3 (182). Available from: https://doi.org/10.3389/fphys.2012.00182.

Plant Life under Changing Environment

References

709

Fischer, G., Shah, M., van Velthuizen, H., Nachtergaele, F.O., 2001. Global Agro-Ecological Assessment for Agriculture in the 21st Century. IIASA and FAO, Laxenburg, Austria. Flexas, J., Bota, J., Loreto, F., Cornic, G., Sharkey, T.D., 2004. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol. 6 (3), 269 279. Flexas, J., Bota, J., Galmes, J., Medrano, H., Ribas-Carbo´, M., 2006. Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol. Plant. 127, 343 352. Frederick, J.R., Camp, C.R., Bauer, P.J., 2001. Drought-stress effects on branch and main stem seed yield and yield components of determinatesoybean. Crop Sci. 41, 759 763. Fu, J., Huang, B., 2001. Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ. Exp. Bot. 45, 105 114. Furbank, R.T., Taylor, W.C., 1995. Regulation of photosynthesis in C3 and C4 plants: a molecular approach. Am. Soc. Plant Physiol. 7, 797 807. Fares, S., Barta, C., Brilli, F., Centritto, M., Ederli, L., Ferranti, F., et al., 2006. Impact of high ozone on isoprene emission, photosynthesis and histology of developing Populus alba leaves directly or indirectly exposed to the pollutant. Physiol. Plant. 128, 456 465. Foyer, C., Noctor, G., 2005. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 28, 1056 1071. Frei, M., 2015. Breeding of ozone resistant rice: relevance, approaches and challenges. Environ. Pollut. 197, 144 155. Gai, Y.P., Li, X.Z., Ji, X.L., Wu, C.A., Yang, G.D., Zheng, C.-C., 2008. Chilling stress accelerates degradation of seed storage protein and photosynthetic protein during cotton seed germination. J. Agron. Crop Sci. 194, 278 288. Galme´s, J., Abadı´a, A., Cifre, J., Medrano, H., Flexas, J., 2007. Photoprotection processes under water stress and recovery in Mediterranean plants with different growth forms and leaf habits. Physiol. Plant. 130, 495 510. Galme´s, J., Ribas-Carbo´, M., Medrano, H., Flexas, J., 2010. Rubisco activity in Mediterranean species is regulated by the chloroplastic CO2 concentration under water stress. J. Exp. Bot. 62, 653 665. Gao, F., Zhou, Y., Zhu, W., Li, X., Fan, L., Zhang, G., 2009. Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230, 1033 1046. Gil, R., Boscaiu, M., Lull, C., Bautista, I., Lido´n, A., Vicente, O., 2013. Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Funct. Plant Biol. 40, 805 818. Gime´nez, C., Mitchell, V.J., Lawlor, D.W., 1992. Regulation of photosynthesis rate of two sunflower hybrids under water stress. Plant Physiol. 98, 516 524. Grace, J., 1999. Environmental controls of gas exchange in tropical rain forests. In: Press, M.C., Scholes, J.D., Barker, M.G. (Eds.), Physiological Plant Ecology. British Ecological Society, London, UK. Gregg, J., Jones, C., Dawson, T., 2003. Urbanization effects on tree growth in the vicinity of New York City. Nature 424, 183 187. Grzyb, J., Waloszek, A., Latowski, D., Wieckowski, S., 2004. Effect of cadmium on ferredoxin: NADP1 oxidoreductase activity. J. Inorg. Biochem. 98, 1338 1346. Gunasekera, D., Berkowitz, G.A., 1993. Use of transgenic plants with Rubisco antisense DNA to evaluate the rate limitation of photosynthesis under water stress. Plant Physiol. 103, 629 635. Gupta, D.K., Chatterjee, S. (Eds.), 2017. Arsenic Contamination in the Environment: The Issues and Solutions. Springer International Publishing, AG Switzerland. Available from: https://doi.org/10.1007/978-3-319-54356-7. Gupta, B.K., Sahoo, K.K., Ghosh, A., Tripathi, A.K., Anwar, K., Das, P., et al., 2017. Manipulation of glyoxalase pathway confers tolerance to multiple stresses in rice. Plant Cell Environ. Available from: https://doi.org/ 10.1111/pce.12968. Ha, C.V., Leyva-Gonzalez, M.A., Osakabe, Y., Tran, U.T., Nishiyama, R., Watan-Abe, Y., et al., 2014. Positive regulatory role of strigolactonein plant responses to drought and salt stress. Proc. Natl. Acad. Sci. U.S.A. 111, 581 856. Haa, C.V., Leyva-Gonza´lezc, M.A., Osakabed, Y., Trana, U.T., Nishiyamaa, R., Watanabea, Y., et al., 2014. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc. Natl. Acad. Sci. U.S.A. 111, 851 856. Hancock, R.D., Morris, W.L., Ducreux, L.J., Morris, J.A., Usman, M., Verrall, S.R., et al., 2014. Physiological, biochemical and molecular responses of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ. 37, 439 450. Harrison, E.P., Willingham, N.M., Lloyd, J.C., Raines, C.A., 1997. Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204, 27 36.

Plant Life under Changing Environment

710

27. Regulation of the Calvin cycle under abiotic stresses: an overview

Hasanuzzaman, M., Nahar, K., Alam, M.M., Roychowdhury, R., Fujita, M., 2013. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 14, 9643 9684. Hayano-Kanashiro, C., Caldero´n-Va´zquez, C., Ibarra-Laclette, E., Herrera-Estrella, L., Simpson, J., 2009. Analysis of gene expression and physiological responses in three Mexican maize landraces under drought stress and recovery irrigation. PLoS One 4, e7531. He, J., Huang, L.-K., Chow, W.S., Whitecross, M.I., Anderson, J.M., 1993. Effects of supplementary ultraviolet-B radiation on rice and pea plants. Aust. J. Plant Physiol. 20, 129 142. He, J., Huang, L.K., Whitecross, M.I., 1994. Chloroplast ultra structure changes in Pisum sativum associated with supplementary ultraviolet (UV-B) radiation. Plant Cell Environ 17, 771 775. He, Y., Yu, C.L., Zhou, L., Chen, Y., Liu, A., Jin, J.H., et al., 2014. Rubisco decrease is involved in chloroplast protrusion and Rubisco-containing body formation in soybean (Glycine max) under salt stress. Plant Physiol. Biochem. 74, 118 124. Heath, R.L., 2008. Modification of the biochemical pathways of plants induced by ozone: what are the varied routes to change? Environ. Pollut. 155, 453 463. Heidarvand, L., Maali-Amiri, R., 2010. What happens in plant molecular responses to cold stress? Acta Physiol. Plant. 32, 419 431. Herrera, A., 2013. Responses to flooding of plant water relations and leaf gas exchange in tropical tolerant trees of a black-water wetland. Front. Plant Sci. 4, 106. Available from: https://doi.org/10.3389/fpls.2013.00106. Hideg, E., Kalai, T., Hideg, K., Vass, I., 2000. Do oxidative stress conditions impairing photosynthesis in the light manifest as photoinhibition? Phil Trans. Roy. Soc. Lond. B 355, 1511 1516. Hoang, T.M., Tran, T.N., Nguyen, T.K., et al., 2016. Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy 6, 54. Hollo´sy, F., 2002. Effects of ultraviolet radiation on plant cells. Micron 33, 179 197. Hossain, Z., Lo´pez-Climent, M.F., Arbona, V., Pe´rez-Clemente, R.M., Go´mez-Cadenas, A., 2009. Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage. J. Plant Physiol. 166, 1391 1404. Hove-Jensen, B., Maigaard, M., 1993. Escherichia coli rpiA gene encoding ribose phosphate isomerase A. J. Bacteriol. 175, 5628 5635. Hu, X., Wu, L., Zhao, F., Zhang, D., Li, N., Zhu, G., et al., 2015. Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress. Front. Plant Sci. 6, 1 21. Iglesias-Ferna´ndez, R., Matilla, A.J., 2016. Flooding stress and O2-shortage in plants. In: Ahmad, Parvaiz (Ed.), Water Stress and Crop Plants: A Sustainable Approach, vol. 1. About Wiley Online Library Ctfhapter 41. Available from: https://doi.org/10.1002/9781119054450.ch41. James, R.A., Munns, R., von Caemmerer, S., Trejo, C., Miller, C., Condon, T.A.G., 2006. Photosynthetic capacity is related to the cellular and subcellular partitioning of Naþ, Kþ and Cl- in salt-affected barley and durum wheat, Plant Cell Environ., 29. pp. 2185 2197. Jedmowski, C., Bayramov, S., Bru¨ggemann, W., 2014. Comparative analysis of drought stress effects on photosynthesis of Eurasian and North African genotypes of wild barley. Photosynthetica 52, 564 573. Jenkins, G.I., 2017. Photomorphogenic responses to ultraviolet-B light. Plant, Cell Environ. Available from: https://doi.org/10.1111/pce.12934. Jhun, I., Coull, B.A., Zanobetti, A., Koutrakis, P., 2015. The impact of nitrogen oxides concentration decreases on ozone trends in the USA. Air Qual. Atmos. Health 8, 283 292. Jones, H.G., Jones, M.B., 1989. Introduction: some terminology and common mechanisms. In: Jones, H., Flowers, T.J., Jones, M.B. (Eds.), Plants Under Stress, Society for Experimental Biology Seminar Series. Cambridge University Press, Cambridge, pp. 1 10. Jordan, B.R., He, J., Chow, W.S., Anderson, J.M., 1992. Changes in mRNA levels and polypeptide subunits of ribulose-1, 5-bisphosphate carboxylase in response to supplemental UV-B radiation. Plant Cell Environ 15, 91 98. Joshi, R., Karan, R., Singla-Pareek, S.L., et al., 2016a. Ectopic expression of Pokkali phosphoglycerate kinase-2 (OsPGK2-P) improves yield in tobacco plants under salinity stress. Plant Cell Rep. 35, 27 41. Joshi, R., Prashat, R., Sharma, P.C., et al., 2016b. Physiological characterization of gamma-ray induced mutant population of rice to facilitate biomass and yield improvement under salinity stress. Ind. J. Plant Physiol. 21, 545 555. Joshi, R., Sahoo, K.K., Tripathi, A.K., Kumar, R., Gupta, B.K., Pareek, A., et al., 2017. Knockdown of an inflorescence meristem-specific cytokinin oxidase OsCKX2 in rice reduces yield penalty under salinity stress condition. Plant Cell Environ. Available from: https://doi.org/10.1111/pce.12947.

Plant Life under Changing Environment

References

711

Kamal, A.H., Rashid, H., Sakata, K., Komatsu, S., 2015. Gel-free quantitative proteomic approach to identify cotyledon proteins in soybean under flooding stress. J. Proteom. 112, 1 13. Kangasja¨rvi, J., Talvinen, J., Utriainen, M., Karjalainen, R., 1994. Plant defence systems induced by ozone. Plant Cell Environ. 17, 783 794. Kataria, S., Guruprasad, K.N., Ahuja, S., Singh, B., 2013. Enhancement of growth, photosynthetic performance and yield by exclusion of ambient UV components in C3 and C4 plants. J. Photochem. Photobiol. B: Biol. 127, 140 152. Kataria, S., Jajoo, A., Guruprasad, K.N., 2014. Impact of increasing Ultraviolet-B (UV-B) radiation on photosynthetic processes. J. Photochem. Photobiol. B: Biol. 137, 55 66. Khan, I., Ahmad, A., Iqbal, M., 2009. Modulation of antioxidant defence system for arsenic detoxification in Indian mustard. Ecotoxicol. Environ. Saf. 72, 626 634. Khan, N.A., Komatsu, S., Sawada, H., Nouri, M.Z., Kohno, Y., 2013. Analysis of proteins associated with ozone stress response in soybean cultivars. Protein Pept. Lett. 20 (10), 1144 1152. Kicheva, M.I., Tsonev, T.D., Popova, L.P., 1994. Stomatal and non-stomatal limitations to photosynthesis in two wheat cultivars subjected to water stress. Photosynthetica 30, 107 116. Kim, S.Y., Lim, J.H., Park, M.R., Kim, Y.J., Park, T., Seo, Y.W., et al., 2005. Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. J. Biochem. Mol. Biol. 38, 218 224. Kimball, S.L., Salisbury, F.B., 1973. Ultrastructural changes of plants exposed to low temperatures. Am. J. Bot. 60, 1028 1033. Kirschbaum, M.U.F., 1988. Recovery of photosynthesis from water stress in Eucalyptus pauciflora—a process in two stages. Plant Cell Environ. 11, 685 694. Kohlhoff, M., Dahm, A., Hensel, R., 1996. Tetrameric triosephosphate isomerase from hyperthermophilic Archaea. FEBS Lett. 383, 245 250. Kontunen-Soppela, S., Ossipov, V., Ossipova, S., Oksanen, E., 2007. Shift in birch leaf metabolome and carbon allocation during long-term open-field ozone exposure. Global Change Biol. 13, 1053 1067. Kosova, K., Vitamvas, P., Prasil, I.T., Renaut, J., 2011. Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J. Proteome 74, 1301 1322. Kossmann, J., Sonnewald, U., Willmitzer, L., 1994. Reduction of the chloroplastic fructose-16-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J. 6, 637 650. Krapp, A., Hoffman, B., Schafer, C., Stitt, M., 1993. Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for sink regulation of photosynthesis. Plant J. 3, 817 828. Kratsch, H.A., Wise, R.R., 2000. The ultrastructure of chilling stress. Plant Cell Environ. 23, 337 350. Kumari, S., Singh, P., Singla-Pareek, S.L., et al., 2009. Heterologous expression of a salinity and developmentally regulated rice cyclophilin gene (OsCyp2) in E. coli and S. cerevisiae confers tolerance towards multiple abiotic stresses. Mol. Biotechnol. 42, 195 204. Law, B.E., Williams, M., Anthoni, P.M., Baldochi, D.D., Unsworth, M.H., 2000. Measuring and modelling seasonal variation of carbon dioxide and water vapour exchange of a Pinus ponderosa forest subject to soil water deficit. Global Change Biol. 6, 613 630. Lawlor, D.W., 2002. Limitations to photosynthesis in water-stressed leaves: stomatal vs. metabolism and the role of ATP. Ann. Bot. 89, 871 885. Lawlor, D.W., Tezara, W., 2009. Causes of decreased photosynthetic rate and metabolic capacity in waterdeficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann. Bot. 103, 561 579. Lee, D.G., Ahsan, N., Lee, S.H., Kang, K.Y., Bahk, J.D., Lee, I.J., et al., 2007. A proteomic approach in analyzing heat-responsive proteins in rice leaves. Proteomics 7, 3369 3383. Levitt, J., 1980. Responses of Plants to Environmental Stresses, second ed Academic Press, New York. Li, J., Cui, G., Hu, G., Wang, M., Zhang, P., Qin, L., et al., 2017. Proteome dynamics and physiological responses to short-term salt stress in Leymus chinensis leaves. PLoS One 12, e0183615. Li, K., Wang, Y., Han, C., Zhang, W., Jia, H., Li, X., 2007. GA signalling and CO/FT regulatory module mediate salt-induced late flowering in Arabidopsis thaliana. Plant Growth Regul. 53, 195 206. Li, Y.R., Fang, F.X., Wu, J.M., Li, X., Zhang, R.H., Liu, X.H., et al., 2011. Survey of frost and cold damage on sugarcane production in Guangxi in 2010/2011 milling season and countermeasures. J. Southern Agric. 42, 37 42. Lo´pez-Milla´n, A.F., Duy, D., Philippar, K., 2016. Chloroplast iron transport proteins function and impact on plant physiology. Front. Plant Sci. 7, 178.

Plant Life under Changing Environment

712

27. Regulation of the Calvin cycle under abiotic stresses: an overview

Loreto, F., Pinelli, P., Manes, F., Kollist, H., 2004. Impact of ozone on monoterpene emissions and evidences for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex (L.) leaves. Tree Physiol. 24, 361 367. Loreto, F., Schnitzler, J.P., 2010. Abiotic stresses and induced BVOCs. Special Issue: Induced biogenic volatile organic compounds from plants. Trend Plant Sci. 15, 154 166. Lorimer, G.H., 1981. The carboxylation and oxygenation of ribulose-1,5-bisphosphate: the primary event in photosynthesis and photorespiration. Ann. Rev. Plant Physiol. 32, 349 382. Lu, K.X., Cao, B.H., Feng, X.P., He, Y., Jiang, D.A., 2009. Photosynthetic response of salt-tolerant and sensitive soybean varieties. Photosynthetica 47, 381 387. Lu, S.Y., Wang, X.H., Guo, Z.F., 2013. Differential responses to chilling in Stylosanthes guianensis (Aublet) Sw. and its mutants. Agron. J. 105, 377 382. Mahajan, S., Tuteja, N., 2005. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139 158. Majumdar, S., Ghosh, S., Glick, B.R., Dumbroff, E.B., 1991. Activities of chlorophyllase, phosphoenolpyruvatecarboxyllase and ribulose-1,5-bisphosphate carboxylase in the primary leaves of soybean drying senescence and drought. Physiol. Planta 81, 473 480. Maleki, M., Ghorbanpour, M., Kariman, K., 2017. Physiological and antioxidative responses of medicinal plants exposed to heavy metals stress. Plant Gene 11, 247 254. Marian, C.O., Krebs, S.L., Arora, R., 2004. Dehydrin variability among rhododendron species: a 25 kDa dehydrin is conserved and associated with cold acclimation across diverse species. New Phytol. 161, 773 780. Marmiroli, M., Pigoni, V., Savo-Sardaro, M.L., Marmiroli, N., 2014. The effect of silicon on the uptake and translocation of arsenic in tomato (Solanum lycopersicum L.). Environ. Exp. Bot. 99, 9 17. Marques, I.A., Anderson, L.E., 1986. Effects of arsenite, sulfite, and sulfate on photosynthetic carbon metabolism in isolated pea (Pisumsativum L., cv Little Marvel) chloroplasts. Plant Physiol. 82, 488 493. Marschner, H., 1995. Mineral Nutrition of Higher Plants, second ed Academic Press, London. Martin, W., Schnarrenberger, C., 1997. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32, 1 18. Martin, W., Henze, K., Kellermann, J., Flechner, A., Schnarrenberger, C., 1996b. Micro-sequencing and cDNA cloning of the Calvin-cycle/OPPP enzyme ribose-5-phosphate isomerase (EC 5.3.1.6) from spinach chloroplasts. Plant Mol. Biol. 30, 795 805. Mandi, S.S., 2016a. Effect of UV radiation on life forms. In: Mandi, S.S. (Ed.), Natural UV Radiation in Enhancing Survival Value and Quality of Plants. Springer, New Delhi, India, pp. 23 43. Mandi, S.S., 2016b. UV radiation-induced damage at molecular level. In: Mandi, S.S. (Ed.), Natural UV Radiation in Enhancing Survival Value and Quality of Plants. Springer, New Delhi, India, pp. 45 71. Manes, F., Donato, E., Vitale, M., 2001. Physiological response of Pinus halepensis needles under ozone and water stress conditions. Physiol. Plant. 113, 249 257. Mauser, H., King, W.A., Gready, J.E., Andrews, T.J., 2001. CO2 fixation by Rubisco: computational dissection of the key steps of carboxylation, hydration, and C C bond cleavage. J. Am. Chem. Soc. 123, 10821 10829. McAdam, E.L., Brodribb, T.J., McAdam, S.A., 2017. Does ozone increase ABA levels by non-enzymatic synthesis causing stomata to close? Plant Cell Environ. 40, 741 747. Mehta, R.A., Fawcett, T.W., Porath, D., Mattoo, A.K., 1992. Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase. J. Biol. Chem. 267, 2810 2816. Melis, A., Nemson, J.A., Harrison, M.A., 1992. Damage to functional components and partial degradation of photosystem II reaction centre proteins upon chloroplast exposure to ultraviolet-B radiation. Biochimica et Biophysica Acta 1109, 312 320. Mitra, A., Chatterjee, S., Moogouei, R., Gupta, D.K., 2017. Arsenic accumulation in rice and probable mitigation approaches: a review. Agronomy 7, 67. Available from: https://doi.org/10.3390/agronomy7040067. Mittal, S., Kumari, N., Sharma, V., 2012. Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant. Physiol. Biochem. 54, 17 26. Miura, K., Furumoto, T., 2013. Cold signalling and cold response in plants. Int. J. Mol. Sci. 14, 5312 5337. Miyashita, K., Tanakamaru, S., Maitani, T., Kimura, K., 2005. Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environ. Exp. Bot. 53, 205 214. Montreal Protocol (1987) ,http://www.iifiir.org/userfiles/file/webfiles/regulation_files/Montreal_EN.pdf .. Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant. Biol. 59, 651 681.

Plant Life under Changing Environment

References

713

Munns, R., James, R., Lauchli, A., 2006. Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57, 1025 1043. Mustafa, G., Komatsu, S., 2016. Toxicity of heavy metals and metal-containing nanoparticles on plants. Biochim. Biophys. Acta 1864, 932 944. Mutava, R.N., Prince, S.J.K., Syed, N.H., Song, L., Valliyodan, B., Chen, W., et al., 2015. Understanding abiotic stress tolerance mechanisms in soybean: a comparative evaluation of soybean response to drought and flooding stress. Plant Physiol. Biochem. 86, 109 120. Nie, G.Y., Tomasevic, M., Baker, N.R., 1993. Effects of ozone on the photosynthetic apparatus and leaf proteins during leaf development in wheat. Plant Cell Environ. 16, 643 651. Nogues, S., Baker, N.R., 1995. Evaluation of the role of damage to photosystem II in the inhibition of CO2 assimilation in pea leaves on exposure to UV-B radiation. Plant Cell Environ 18, 781 787. Nouri, M.Z., Moumeni, A., Komatsu, S., 2015. Abiotic stresses: insight into gene regulation and protein expression in photosynthetic pathways of plants. Int. J. Mol. Sci. 16, 20392 20416. Ort, D.R., Baker, N.R., 2002. A photoprotective for O2 as an alternative electron sink in photosynthesis. Curr. Opin. Plant. Biol. 5, 193 198. Osakabe, K., Osakabe, Y., 2012. Plant light stress. In: Robinson, S.A. (Ed.), Encyclopaedia of Life Sciences. Nature Publishing Group, London, ed. Pankovic, D., Sakac, Z., Kevresan, S., Plesnicar, M., 1999. Acclimation to long-term water deficit in the leaves of two sunflower hybrids: photosynthesis, electron transport and carbon metabolism. J. Exp. Bot. 50, 127 138. Paoletti, E., Paoletti, E., Schaub, M., Matyssek, R., Wieser, G., Augustaitis, A., et al., 2010. Advances of air pollution science: from forest decline to multiple-stress effects on forest ecosystem services. Environ. Pollut. 158, 1986 1989. Parida, A.K., Das, A.B., 2005. Salt tolerance and salinity effect on plants: a review. Ecotoxicol. Environ. Saf. 60, 324 349. Parry, M.A.J., Andralojc, P.J., Khan, S., Lea, P.J., Keys, A.J., 2002. Rubisco activity: effects of drought stress. Ann. Bot. 89, 833 839. Parry, M.A.J., Keys, A.J., Madgwick, P.J., Carmo-Silva, A.E., Andralojc, P.J., 2008. Rubisco regulation: a role for inhibitors centre. J. Exp. Bot. 59, 1569 1580. Pell, E.J., Landry, L.G., Eckardt, N.A., Click, R.E., 1994. Effects of gaseous air pollutants on ribulose bisphosphate carboxylase/oxygenase: effects and implications. In: Alscher, R.G., Wellburn, A.R. (Eds.), Plant Response to the Gaseous Environment: Molecular, Metabolic and Physiological Aspects. Chapman and Hall, London, UK, pp. 239 254. Pell, E.J., Schlagnhaufer, C.D., Arteca, R.N., 1997. Ozone-induced stress: mechanisms of action and reaction. Physiol. Plant. 100, 264 273. Pelloux, J., Jolivet, Y., Fontaine, V., Banvoy, J., Dizengremel, P., 2001. Changes in Rubisco and Rubisco activase gene expression and polypeptide content in Pinushalepensis M. subjected to ozone and drought. Plant Cell Environ. 24, 123 131. Penfield, S., 2008. Temperature perception and signal transduction in plants. New Phytol. 179, 615 628. Perdomo, J.A., Capo´-Bauc¸a`, S., Carmo-Silva, E., Galme´s, J., 2017. Rubisco and Rubisco activase play an important role in the biochemical limitations of photosynthesis in rice, wheat, and maize under high temperature and water deficit. Front. Plant Sci. 8, 490. Pettigrew, W.T., 2004. Physiological consequences of moisture deficit stress in cotton. Crop Sci. 44, 1265 1272. Pinheiro, C., Chaves, M.M., 2011. Photosynthesis and drought: can we make metabolic connections from available data? J. Exp. Bot. 62, 869 882. Pinheiro, C., Kehr, J., Ricardo, C.P., 2005. Effect of water stress on lupin stem protein analysed by twodimensional gel electrophoresis. Planta 221, 716 728. Pourrut, B., Shahid, M., Dumat, C., Winterton, P., Pinelli, E., 2011. Lead uptake, toxicity, and detoxification in plants. Rev. Environ. Contamin. Toxic. 213, 113 136. Prado, F.E., Rosa, M., Prado, C., Podazza, G., Interdonato, R., Gonza´lez, J.A., Hilal, M., 2012. UV-B radiation, its effects and defense mechanisms in terrestrial plants. In: Ahmad, P., Prasad, M.N.V. (Eds.), Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. Springer, The Netherlands, pp. 57 83. Purty, R.S., Kumar, G., Singla-Pareek, S.L., et al., 2008. Towards salinity tolerance in Brassica: an overview. Physiol. Mol. Biol. Plants 14, 39 49.

Plant Life under Changing Environment

714

27. Regulation of the Calvin cycle under abiotic stresses: an overview

Qureshi, M.I., Abdin, M.Z., Ahmad, J., Iqbal, M., 2013. Effect of long-term salinity on cellular antioxidants, compatible solute and fatty acid profile of sweet annie (Artemisia annua L.). Phytochemistry 95, 215 223. Raines, C.A., Harrison, E.P., Olcer, H., Lloyd, J.C., 2000. Investigating the role of the thiol-regulated enzyme sedoheptulose-1,7-bisphosphatase in the control of photosynthesis. Physiol. Plant. 110, 303 308. Razavizadeh, R., Ehsanpour, A.A., Ahsan, N., Komatsu, S., 2009. Proteome analysis of tobacco leaves under salt stress. Peptides 30, 1651 1659. Reddy, A.R., Chaitanya, K.V., Vivekanandan, M., 2004. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J. Plant Physiol. 161, 1189 1202. Renaut, J., Hoffmann, L., Hausman, J.F., 2005. Biochemical and physiological mechanisms related to cold acclimation and enhanced freezing tolerance in poplar plantlets. Physiol. Plant. 125, 82 94. Rı´o Segade, S., Vilanova, M., Giacosa, S., Perrone, I., Chitarra, W., Pollon, M., et al., 2017. Ozone improves the aromatic fingerprint of white grapes. Sci. Rep. 24, 16301. Available from: https://doi.org/10.1038/s41598017-16529-5. Rokka, A., Zhang, L., Aro, E., 2001. Rubisco activase: an enzyme with a temperature-dependent dual function? Plant J. 25, 463 471. Ruelland, E., Vaultier, M.N., Zachowski, A., Hurry, V., 2009. Cold signalling and cold acclimation in plants. In: Jean-Claude, K., Michel, D. (Eds.), Advances in Botanical Research, vol. 49. Academic Press, pp. 35 150. Sakamoto, W., 2006. Protein degradation machineries in plastids. Annu. Rev. Plant. Biol. 57, 599 621. Sanda, S., Yoshida, K., Kuwano, M., Kawamura, T., Munekage, Y.N., Akashi, K., et al., 2011. Responses of the photosynthetic electron transport system to excess light energy caused by water deficit in wild watermelon. Physiol. Plant. 142, 247 264. Sanglard, L.M.V.P., Detmann, K.C., Martins, S.C.V., Teixeira, R.A., Pereira, L.F., Sanglard, M.L., et al., 2016. The role of silicon in metabolic acclimation of rice plants challenged with arsenic. Environ. Exp. Bot. 123, 22 36. Scafaro, A.P., Haynes, P.A., Atwell, B.J., 2010. Physiological and molecular changes in Oryza meridionalis Ng, a heat-tolerant species of wild rice. J. Exp. Bot. 61, 191 202. Schnarrenberger, C., Flechner, A., Martin, W., 1995. Enzymatic evidence indicating a complete oxidative pentose phosphate in the chloroplasts and an incomplete pathway in the cytosol of spinach leaves. Plant Physiol. 108, 609 614. Semenov, M.A., Halford, N.G., 2009. Identifying target traits and molecular mechanisms for wheat breeding under a changing climate. J. Exp. Bot. 60, 2791 2804. Shahid, M., Shamshad, S., Rafiq, M., Khalid, S., Bibi, I., Niazi, N.K., et al., 2017. Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178, 513 533. Sharma, S., Chatterjee, S., Kataria, S., Joshi, J., Datta, S., Vairale, M.G., et al., 2017. A review on responses of plants to UV-B radiation related stress. In: Singh, V.P., Singh, S., Prasad, S.M., Parihar, P. (Eds.), UV-B Radiation: From Environmental Stressor to Regulator of Plant Growth. John Wiley Sons, New York, pp. 75 97. Available from: https://doi.org/10.1002/9781119143611, Ch. 5. Sharmila, P., Kumari, P.K., Singh, K., Prasad, N.V.S.R.K., Pardha-Saradhi, P., 2017. Cadmium toxicity-induced proline accumulation is coupled to iron depletion. Protoplasma 254, 763 770. Sharmin, S.A., Alam, I., Rahman, M.A., Kim, K.H., Kim, Y.G., Lee, B.H., 2013. Mapping the leaf proteome of Miscanthus sinensis and its application to the identification of heat-responsive proteins. Planta 238, 459 474. Sharp, R.E., 2002. Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ. 25, 211 222. Shavrukov, Y., Kurishbayev, A., Jatayev, S., et al., 2017. Early flowering as a drought escape mechanism in plants: how can it aid wheat production? Front. Plant Sci. 8, 1950. Available from: https://doi.org/10.3389/fpls.2017.01950. Sheen, J., 1990. Metabolic repression to transcription in higher plants. Plant Cell 2, 1027 1038. Shi, Y., Ding, Y., Yang, S., 2015. Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiol. 56, 7 15. Shu, K., Zhang, H., Wang, S., Chen, M., Wu, Y., Tang, S., et al., 2013. ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet. 9, e1003577. Siedlecka, A., Krupa, Z., Samuelsson, G., Oquist, G., Gardestrom, P., 1997. Primary carbon metabolism in Phaseolus vulgaris plants under Cd/Fe interaction. Plant. Physiol. Biochem. 35, 951 957. Singh, J., Pandey, P., James, D., Chandrasekhar, K., Achary, V.M., Kaul, T., et al., 2014. Enhancing C3 photosynthesis: an outlook on feasible interventions for crop improvement. Plant. Biotechnol. J. 12 (9), 1217 1230.

Plant Life under Changing Environment

References

715

Singh, M., Kushwaha, B.K., Singh, S., Kumar, V., Singh, V.P., Prasad, S.M., 2017. Sulphur alters chromium (VI) toxicity in Solanummelongena seedlings: role of sulphur assimilation and sulphur-containing antioxidants. Plant. Physiol. Biochem. 112, 183 192. Sipka, G., Kis, M., Maro´ti, P., 2017. Characterization of mercury(II)-induced inhibition of photochemistry in the reaction center of photosynthetic bacteria. Photosynth. Res. Available from: https://doi.org/10.1007/s11120-017-0474-8. Sobhanian, H., Aghaei, K., Komatsu, S., 2011. Changes in the plant proteome resulting from salt stress: toward the creation of salt-tolerant crops? J. Proteomics 74, 1323 1337. Solomon, S., Rosenlof, K., Portmann, R., Daniel, J., Davis, S., Sanford, T., et al., 2010. Contributions of stratospheric water vapor to decadal changes in the rate of global warming. Science 327, 1219 1223. Spreitzer, R.J., Salvucci, M.E., 2002. Rubisco: structure, regulatory interactions and possibilities for a better enzyme. Annu. Rev. Plant. Biol. 53, 449 475. Stoeva, N., Bineva, T., 2003. Oxidative changes and photosynthesis in Oat plants grown in As contaminated soil. Bulg. J. Plant Physiol. 29, 87 95. Su, F., Jacquard, C., Villaume, S., Michel, J., Rabenoelina, F., Cle´ment, C., et al., 2015. Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana. Front. Plant Sci. 6, 810. Sudhir, P., Murthy, S.D.S., 2004. Effect of salt stress on basic processes of photosynthesis. Photosynthetica 42, 481 486. Sugiyama, T., Mizuno, M., Hayashi, M., 1984. Partitioning of nitrogen among ribulose-1,5-bisphosphate carboxylase/oxygenase, phosphoenolpyruvate carboxylase, and pyruvate orthophosphate dikinase as related to biomass productivity in maize seedlings. Plant Physiol. 75, 665 669. Suzuki, K., Nagasuga, K., Okada, M., 2008. The chilling injury induced by high root temperature in the leaves of rice seedlings. Plant Cell Physiol. 49, 433 442. Tabita, F.R., 1988. Molecular and cellular regulation of autotrophic carbon-dioxide regulation in microorganisms. Microbiol. Rev. 52, 155 189. Tabita, F.R., 1994. The biochemistry and molecular regulation of carbon dioxide metabolism in cyanobacteria. In: Bryant, D.A. (Ed.), The Molecular Biology of Cyanobacteria. Kluwer, Dordrecht, pp. 437 467. Taiz, L., Zeiger, E., 2006. Plant Physiology, fourth ed. Sinauer Associates Inc. Publishers, Sunderland, MA. Taiz, L., Zeiger, E., 2014. sixth revised ed. Plant Physiology and Development:, 2014. Sinauer Associates Inc, Sunderland, MA. Takeuchi, A., Yamaguchi, T., Hidema, J., Strid, A., Kumagai, T., 2002. Changes in synthesis and degradation of Rubisco and LHCII with leaf age in rice (Oryza sativa L.) growing under supplementary UV-B radiation. Plant Cell Environment 25, 695 706. Tezara, W., Lawlor, D.W., 1995. Effects of water stress on the biochemistry and physiology of photosynthesis in sunflower. In: Mathis, P. (Ed.), Photosynthesis: From Light to Biosphere IV. Kluwer Academic Publishers, Dordrecht, pp. 625 628. Tezara, W., Mitchell, V.J., Driscoll, S.D., Lawlor, D.W., 1999. Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401, 914 917. Tezara, W., Mitchell, V., Driscoll, S.P., Lawlor, D.W., 2002. Effects of water deficit and its interaction with CO2 supply on the biochemistry and physiology of photosynthesis in sunflower. J. Exp. Bot. 53, 1781 1791. Theocharis, A., Bordiec, S., Fernandez, O., Paquis, S., Dhondt-Cordelier, S., Baillieul, F., et al., 2012. Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol. Plant Microbe Interact. 25, 241 249. Thwe, A.A., Vercambre, G., Gautier, H., Gay, F., Phattaralerphong, J., Kasemsap, P., 2015. Effects of acute ozone stress on reproductive traits of tomato, fruit yield and fruit composition. J. Sci. Food. Agric. 95, 614 620. To´th, T., Zsiros, O., Kis, M., Garab, G., Kova´cs, L., 2012. Cadmium exerts its toxic effects on photosynthesis via a cascade mechanism in the cyanobacterium, Synechocystis PCC 6803pce_2537. Plant Cell Environ. 35, 2075 2086. Tournaire-Roux, C., Sutka, M., Javot, H., Gout, E., Gerbeau, P., Luu, D.T., et al., 2003. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425, 393 397. Tripathi, A.K., Pareek, A., Singla-Pareek, S.L., 2016. A NAP-family histone chaperone functions in abiotic stress response and adaptation. Plant Physiol. 171, 2854 2868. Ueda, Y., Siddique, S., Frei, M., 2015. A novel gene, ozone-responsive apoplasticprotein1, enhances cell death in ozone stress in Rice. Plant Physiol. 169, 873 889. Van Assche, F., Clijsters, H., 1990. Effects of metals on enzyme activity in plants. Plant Cell Environ. 13, 195 206.

Plant Life under Changing Environment

716

27. Regulation of the Calvin cycle under abiotic stresses: an overview

Van Dingenen, R., Dentener, F.J., Raes, F., Krol, M.C., Emberson, L., Cofala, J., 2009. The global impact of ozone on agricultural crop yields under current and future air quality legislation. Atmos. Environ. 43, 604 618. Vasellati, V., Oesterheld, M., Medan, D., Loreti, J., 2001. Effects of flooding and drought on the anatomy of Paspalum dilatatum. Ann. Bot. 88, 355 360. Velikova, V., Tsonev, T., Pinelli, P., Alessio, G.A., Loreto, F., 2005. Localized ozone fumigation system for studying ozone effects on photosynthesis, respiration, electron transport rate and isoprene emission in field-grown Mediterranean oak species. Tree Physiol. 25, 1523 1532. Vu, C.V., Allen, L.H., Garrard, L.A., 1984. Effects of UV-B radiation (280 320 nm) on ribulose-1, 5bisphosphate carboxylase in pea and soybean. Environ. Exp. Bot. 24, 131 143. Wang, Y., Nii, N., 2000. Changes in chlorophyll, ribulose bisphosphate carboxylase-oxygenase, glycine betaine content, photosynthesis and transpiration in Amaranthus tricolor leaves during salt stress. J. Hortic. Sci. Biotechnol. 75, 623 627. Wang, D., Pan, Y., Zhao, X., Zhu, L., Fu, B., Li, Z., 2011. Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genom. 12, 149. Wang, X., Dinler, B.S., Vignjevic, M., Jacobsen, S., Wollenweber, B., 2015. Physiological and proteome studies of responses to heat stress during grain filling in contrasting wheat cultivars. Plant Sci. 230, 33 50. Wang, H.B., Xie, F., Yao, Y.Z., Zhao, B., Xiao, Q.Q., Pan, Y.H., et al., 2012. The effects of arsenic and induced-phytoextraction methods on photosynthesis in Pteris species with different arsenic-accumulating abilities. Environ. Exp. Bot. 75, 298 306. Weis, E., 1981. Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151, 33 39. Williams, J., Bulman, M.P., Neill, S.J., 1994. Wilt-induced ABA biosynthesis, gene-expression and down-regulation of rbcS messenger-RNA levels in Arabidopsis thaliana. Physiol. Planta 91, 177 182. Wilson, K.B., Baldocchi, D.D., Hanson, P.J., 2001. Leaf age affects the seasonal pattern of photosynthetic capacity and net ecosystem exchange of carbon in a deciduous forest. Plant Cell Environ. 24, 571 583. Wilson, M., Chosh, S., Cerhardt, K.E., Holland, N., Sudhakar, B.T., Edelman, M., Dumbroff, E.B., Creenberg, B.M., 1995. In Vivo Photomodification of Ribulose-I, 5-Bisphosphate Carboxylase/Oxygenase Holoenzyme by Ultraviolet-B Rad iat ion’ Formation of a 66-Kilodalton Variant of the Large Subunit. Plant Physiol. 109, 221 229. Xin, Z., Browse, J., 2000. Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ. 23, 893 902. Xiong, Z., Zhao, F., Li, M., 2006. Lead toxicity in Brassica pekinensis Rupr.: effect on nitrate assimilation and growth. Environ. Toxicol. 21 (2), 147 153. Yadav, R.S., Hash, C.T., Bidinger, F.R., Devos, K.M., Howarth, C.J., 2004. Genomic regions associated with grain yield and aspects of post flowering drought tolerance in pearl millet across environments and tester background. Euphytica 136, 265 277. Yan, S.P., Zhang, Q.Y., Tang, Z.C., Su, W.A., Sun, W.N., 2006. Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol. Cell. Proteomics 5, 484 496. Zargar, S.M., Kurata, R., Inaba, S., Oikawa, A., Fukui, R., Ogata, Y., et al., 2015. Quantitative proteomics of Arabidopsis shoot microsomal proteins reveals a cross-talk between excess Zn and iron deficiency. Proteomics 15, 1196 1201. Zeng, Z.Z., Wei, J., Wei, R.H., Zhu, X.Q., 2008. Investigation of frost bitten sugarcane in Liujiang County. In: Proceedings of Annual Meeting of Guangxi Society of Sugarcane Technologists, pp. 189 192. Zhang, L., Zhang, L., Sun, J., Zhang, Z., Ren, H., Sui, X., 2013. Rubisco gene expression and photosynthetic characteristics of cucumber seedlings in response to water deficit. Sci. Hortic. 161, 81 87. Zhang, B.Q., Yang, L.T., Li, Y.R., 2015a. Physiological and biochemical characteristics related to cold resistance in sugarcane. Sugar Tech 17, 49 58. Zhang, S., Zhu, S., Wu, P., Chen, Y., et al., 2015b. Global analysis of gene expression profiles in physic nut (Jatropha curcas L.) seedlings exposed to drought stress. BMC Plant Biol. 21, 15 17. Zhang, Y.M., Ma, H.L., Caldero´n-Urrea, A., et al., 2016. Anatomical changes to protect organelle integrity account for tolerance to alkali and salt stresses in Melilotus officinalis. Plant Soil 406, 327 340. Zhang, T., Lu, Q., Su, C., Yang, Y., Hu, D., Xu, Q., 2017. Mercury induced oxidative stress, DNA damage, and activation of antioxidative system and Hsp70 induction in duckweed (Lemna minor). Ecotoxicol. Environ. Saf. 143, 46 56. Available from: https://doi.org/10.1016/j.ecoenv.2017.04.058.

Plant Life under Changing Environment

Further reading

717

Zheng, Y., Shimizu, H., Barnes, J.D., 2002. Limitations to CO2 assimilation in ozone-exposed leaves of Plantago major. New Phytol. 155, 67 78. Zhou, Y., Lam, H.M., Zhang, J., 2007. Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J. Exp. Bot. 58, 1207 1217. Zhu, J., Dong, C.H., Zhu, J.K., 2007. Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr. Opin. Plant Biol. 10, 290 295. Ziska, L.H., Seemann, J.R., Dejong, T.M., 1990. Salinity induced limitations on photosynthesis in Prunus salicina, a deciduous tree species. Plant Physiol. 93, 864 870.

Further reading Banks, F.M., Driscoll, S.P., Parry, M.A.J., Lawlor, D.W., Knight, J.S., Gray, J.C., et al., 1999. Decrease in phosphoribulokinase activity by antisense RNA in transgenic tobacco. Relationship between photosynthesis, growth and allocation at different nitrogen levels. Plant Physiol. 119, 1125 1136. Bassham, J., Benson, A., Calvin, M., 1950. The path of carbon in photosynthesis. J. Biol. Chem. 185 (2), 781 787. PMID: 14774424. Comont, D., Winters, A., Gomez, L.D., McQueen-Mason, S.J., Gwynn-Jones, D., 2013. Latitudinal variation in ambient UV-B radiation is an important determinant of Lolium perenne forage production, quality, and digestibility. J. Exp. Bot. 64, 2193 2204. Jansen, M.A., Gaba, V., Greenberg, B.M., 1998. Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci. 3, 131 135. Paul, M.J., Knight, J.S., Habash, D., Parry, M.A.J., Lawlor, D.W., Barnes, S.A., et al., 1995. Reduction in phosphoribulokinase activity by antisense RNA in transgenic tobacco: effect on CO2 assimilation and growth at low irradiance. Plant J. 7, 535 542. Wise, R.R., 1995. Chilling-enhanced photooxidation: the production, action and study of reactive oxygen species produced during chilling in the light. Photosynth. Res. 45, 79 97.

Plant Life under Changing Environment

C H A P T E R

28 Roles of microRNAs in plant development and stress tolerance Vaishali Yadav1, Namira Arif1, Vijay Pratap Singh2, Rupesh Deshmukh3, Shivendra Sahi4, S.M. Shivaraj5,6, Durgesh Kumar Tripathi7 and Devendra Kumar Chauhan1 1

D D Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Prayagraj, India 2Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, India 3National Agri-Food Biotechnology Institute (NABI), Mohali, India 4University of the Sciences in Philadelphia (USP), Philadelphia, PA, United States 5Laval University, Quebec City, QC, Canada 6National Research Centre on Plant Biotechnology, New Delhi, India 7Amity Institute of Organic Agriculture, Amity University Uttar Pradesh, Noida, India

28.1 Introduction Small RNAs are single-stranded noncoding RNA molecules of B20
30 nucleotides (Kim et al., 2009) known to play a significant role in several cellular mechanisms. These small RNAs comprised small-interference RNAs (siRNAs), microRNAs (miRNAs), and PIWI (P element
induced wimpy testis)-interacting RNAs (piRNAs) (Felekkis et al., 2010). The small RNAs regulate gene expression at the transcriptional and posttranscriptional level, and the whole mechanism of gene regulation by small RNAs is referred to as RNA interference (Agrawal et al., 2003). Among small RNAs, miRNAs and siRNAs are found in majority of the eukaryotes (Bartel, 2004; Shabalina and Koonin, 2008; Carthew and Sontheimer, 2009), while piRNAs are found only in animals (Kim, 2006). miRNAs are an evolutionarily conserved group of B22 nucleotides longendogenous noncoding RNAs, which control the gene expressions (Mette et al., 2000), while post-transcriptionally via either transcript cleavage, translation repression, or both (Bartel, 2004). It is becoming apparent that miRNAs assist various regulatory mechanisms such as developmental timing, host
pathogen interaction, cell differentiation, cell

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28. Roles of microRNAs in plant development and stress tolerance

proliferation, apoptosis as well as tumorigenesis (Cai et al., 2009). miRNA acts as a regulatory element and is modulated by various effectors such as SNP, miRNA editing, methylation, and circadian clock (Cai et al., 2009). In plants, miRNAs regulate various growth and developmental processes such as root development, morphogenesis of leaf, and floral organ identity. miRNAs are also involved in signal transduction and regulate the expression of stress-responsive genes (Zhang et al., 2006), thereby protecting plants during adverse environmental conditions such as salinity, drought, cold stress as well as heavy-metal stress, which lead to oxidative stress (Shriram et al., 2016). In the past few decades, the field of miRNA research experienced the lack of specific methodologies for miRNA identification and characterization. However, with several technical advancements, a significant progress has been made in understanding the role of miRNAs in plant development and stress tolerance. The abiotic stress in crop plants emerged as a major challenge affecting sustainable crop production. In the present book chapter, we have discussed biogenesis and the role of miRNAs in plant development and abiotic stresses.

28.2 Biogenesis of microRNAs miRNAs are encoded by several genomic loci, which may be intronic or intergenic in nature (MacFarlane and Murphy, 2010). Intronic miRNAs are transcribed from the same promoter with their analogous encoded genomic sequence, spliced and processed into mature miRNA, while the intergenic miRNAs are transcribed by the genomic sequences within their own promoter region (Olena and Patton, 2010). In plants, such as Arabidopsis, the transcription and maturation of miRNA through the miRNA genes are a synchronized mechanism, in which miRNA genomic sequences encode a several nucleotide long primary miRNA (pri-miRNA) by the active participation of Pol II enzymes (Grennan, 2008). In plants and animals, miRNA synthesized from the long single-stranded RNAs that fold and form double-stranded hairpin RNAs called pri-miRNAs (Wahid et al., 2010). In the nucleus, two cuts mediated by RNAse III type of endonuclease, Dicer-like 1 (DCL1) liberate the miRNA:miRNA* duplex from pri-miRNAs. Several proteins such as HYPONASTIC LEAVES1 (HYL1), nuclear cap-binding complex, SERRATE (SE), and DAWDLE assist DCL1 for accurate processing of miRNAs (Cho et al., 2016). The double-stranded RNAbinding protein HYL1 and SE assist in loading and positioning of pri-miRNA to DCL1 during processing (Fang and Spector, 2007). After processing, a methyltransferase, HEN1 adds methyl groups to miRNA:miRNA* duplex strands, imparting stability to the miRNA molecule (Yu et al., 2005; Yang et al., 2006). The methylated miRNA:miRNA* duplex is exported into the cytoplasm, where the miRNA:miRNA* duplex is loaded into the RNAinduced silencing complex (RISC) (Chen, 2005; Cho et al., 2016), and miRNA* is degraded (Schwarz et al., 2003). The core component of RISC complex is the ARGONAUTE1 protein, which possesses two domains: 20 kDa N-terminal PAZ domain, which binds the 30 end of ssRNA molecule by a hydrophilic cleft and the 40 kDa C-terminal PIWI domain, which shows structural resemblance to RNase H, which has endonuclease activity (Ho¨ck and Meister, 2008). RISC-loaded miRNAs directs the RISC to regulate the gene expression either by mRNA cleavage or translational repression (Eamens et al., 2009).

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In plants, miRNA binds to target mRNAs at complementary site and directs cleavage of target mRNA (Chen, 2005). Majority of miRNAs targets include the transcription factors, which play crucial role in the hormonal signaling, metabolism, cellular differentiation, flowering and regeneration, nutrient homeostasis, and stress responses (Sun et al., 2015; Hong and Jackson, 2015; Tripathi et al., 2015).

28.3 Role of microRNAs in plant growth and development Plant miRNAs actively participate in the plant growth, development, and cellular metabolism (Yang et al., 2013; Xie et al., 2007). Several works related to miRNAs suggested the involvement of miRNAs in leaf development, apical dominancy, and biomass production as well as in increasing crop yield (Zhang et al., 2015). The role of miRNAs in plant development can be analyzed by two different ways: first through the study of genes necessary for miRNA biogenesis and second, through the identification of miRNA-targeted genomic sequences (Carrington and Ambros, 2003). The dcl mutants showed reduced accumulation of functional miRNAs. The dcl mutant plants show overproliferation of meristematic cells, conversion of floristic meristem into the indeterminate meristematic tissues, as well as delay flowering time and overproliferation of embryonic suspensor cells (Schauer et al., 2002; Reinhart et al., 2002). Mutants in other genes that are required for the miRNAs synthesis, such as HEN1 and AGO1, cause polarity defects in leaf (Park et al., 2002). Mutation in AGO1 resulted in the loss of both domains named PAZ and PIWI, due to which seedlings germinated but meristem did not function properly, which resulted in radial and sterile plants (Ho¨ck and Meister, 2008) whereas mutation in only PIWI domain plants shows weaker phenotype with adaxialized organs, but the plants are fertile to some extent (Kidner and Martienssen, 2004). hen1 and hyl1 mutants exhibit weaker phenotype in comparison to dcl1 mutants. hyl1 mutant plants affect the leaf formation, apical dominancy, and hormonal regulation (Lu and Fedoroff, 2000). This mutant gene increased the abscisic acid sensitivity and decreased the impacts of cytokinin and auxin (Lu and Fedoroff, 2000), while the absence or complete loss of HEN1 and HYL1 activity causes phenotypic defects in plants, which are much less brutal to ago1 and dcl1 mutants (Kidner and Martienssen, 2004). This analysis suggested that miRNAs are necessary and play a regulatory role in meristem function, organ polarity, floral development, and hormonal regulation. In Arabidopsis thaliana, 83 targeted genomic sequences have been predicted in which 48 miRNA-targeted interactions are validated by the cleavage assay (Jones-Rhoades and Bartel, 2004). Fifteen cleavable sites within target genes were validated through in vivo and in vitro miRNA-guided cleavage assays, and it was also anticipated that miRNAs play a role in “clearing out” regulatory genes during the change of cell’s fate (Jones-Rhoades and Bartel, 2004; Kidner and Martienssen, 2004). These cleavable transcriptional factors regulate meristem recognition, cell division, organ separation, and polarity, which comprises of APETELA2 (AP2), CUP-SHAPED COTYLEDON1 (CUC1) and CUC2, and PHAVOLUTA (PHV) and PHABULOSA (PHB) (Carrington and Ambros, 2003). DCL1 protein is required for miRNA formation, however DCL1 transcripts are in turn regulated by miRNA through negative feedback loop (Chen, 2008). While regulatory functions for desired mRNA cleavage in developmental stage have been documented, conditional

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evidence suggest the regulatory role of miR165/166-guided in the radial patterning of leaves (Rhoades et al., 2002; Tang et al., 2003; Carrington and Ambros, 2003). The transcription factors PHV and PHB are required for the adaxial
abaxial polarity; moreover, these genes are normally expressed in leaf primordial cells present near the shoot meristem to regulate the adaxial cell fate, and the turned-off zone develops the abaxial cell, which is distantly located to the meristem (McConnell et al., 2001). The miR165/166-mediated regulation of PHV and PHB transcription factors involved in adaxial and abaxial fate determination (Merelo et al., 2016). Various phv and phb alleles have substituted nucleotide sequences at the complemented site of miRNA due to which the possibility of phv and phb mRNA cleavages becomes less (McConnell et al., 2001). miR165/mi166 also regulates the axis specification, vascular formation as well as the meristem activity (Merelo et al., 2016). miR164 regulates CUC1 (CUP-SHAPED COTYLEDON1) and CUC2 (CUPSHAPED COTYLEDON2) genes, which are involved in the formation of cell
organ boundaries and also play a positive role in the regulation of SHOOTMERISTEMLESS1 gene (Aida et al., 1999). Leaf development is regulated by the miRJAW. This miRNA also regulates cell division in leaf through the TCP genes (TEOSINTE BRANCHED1, CYCLOIDEA, and PROLIFERATION CELL FACTOR) resulting in the promotion of genes required for DNA replication (Llave et al., 2002). The APETALA2 (AP2) and AP2-like genes play an active role in flowering and floral organ development. The miR172 is known to regulate these genes in different plant species (Krogan et al., 2012; Shivaraj et al., 2014, 2018; Shivaraj and Singh, 2016). miR156, which regulates vegetative phase transition in Arabidopsis and epidermal cell fate in maize through controlling the transcription factors belonging to SQUAMOSA PROMOTER BINDING PROTEIN-LIKE family (Wu et al., 2009). Besides controlling developmental events, miRNAs also regulate the hormonal response. miRNAs target the factors that are necessary for hormone signaling, mainly auxin (Eckardt, 2005). miR167 and miR160 target the auxin-response factor (ARF) genes, and miR393 targets and regulates the TRANSPORT INHIBITOR RESPONSE1 (Bonnet et al., 2004). The miR159 upregulates gibberellic acid and downregulates the DELLA repressor, which is an inhibitor of Gibberellic acid (GA) activity (Achard et al., 2004). The miR159 cleaves the GA-MYB mRNA and also works in the regulation of LEAFY, which is involved in flowering development (Fu, and Harberd., 2003).

28.4 Role of microRNAs in various abiotic stresses Environmental fluctuation causes the production of several miRNAs by plants to cope with these fluctuating conditions (Leung and Sharp, 2010). Various stress-regulated miRNAs are generated under different abiotic-stress conditions such as nutrient imbalance, water stress, cold, salinity, UV-B radiation, and mechanical stress (Khraiwesh et al., 2012). Recently, the expression level of 117 miRNAs has been analyzed in Arabidopsis by using miRNA chips under different stress conditions (Liu et al., 2008; Khraiwesh et al., 2012). Jones-Rhoades and Bartel (2004) reported the stress-induced miRNAs in Arabidopsis; these miRNAs cleaved the target genes such as superoxide dismutases (SODs), laccases, and ATP sulfurylases (APSs). The transcription of miR395 enhanced during sulfate starvation, reducing the accumulation of APSs, APS1, APS3, and APS4, which play important roles in inorganic sulfate assimilation (Ai et al., 2016). Besides the assimilatory genes miR395 also target Plant Life under Changing Environment

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the sulfate transporter gene, ATS68 (Ai et al., 2016). Sunkar and Zhu (2004) identified novel and stress-regulated miRNAs and other small RNAs from Arabidopsis seedlings generated under different abiotic stresses such as cold, water stress, and salinity, and likewise, four miRNA families, miR159, miRNA169, miRNA171, and miRNA172 are induced under abiotic stress in Larix leptolepis, which target MYB, NF-YA, scarecrow as well as transcription factors involved in cell development (Zhang et al., 2010). These miRNAs act as regulators of gene expression through the mRNA cleavage, translational repression, chromatin modeling, and DNA methylation (Zhang et al., 2015). Generally during stress conditions, the upregulated miRNAs downregulate their target mRNA; on the contrary, the downregulated miRNAs lead to the upregulation of their target mRNAs (Chinnusamy et al., 2007).

28.5 MicroRNAs and heavy-metal stress Heavy metals are lethal to plants at high concentration, which affect various physiological and biochemical processes; hence, the plants adopt a complex mechanism to control the exact concentration of heavy metals to minimize their toxic effects (Emamverdian et al., 2015). Recently, several studies reported that miRNAs regulate the target mRNA by posttranscriptional regulation in heavy-metal stress (Gielen et al., 2012). The miR398 controls Cu/Zn SOD (CSD) transcript, which maintains copper homeostasis; similarly, miR393 and miR171 also stabilize the homeostasis of cadmium in cadmium-stressed plants by the negative regulation of the target genes (Ding and Zhu, 2009). Ding et al. (2011) in their experiment, microarray-based analysis of cadmium-responsive miRNAs in rice (Oryza sativa), reported the upregulation of miR528 as well as downregulation of miR162, miR166, miR171, miR390, miR168, and miR156 (Ding et al., 2011). Similar results of miRNA downregulation of miR393, miR171, miR156, and miR396 are shown in another study on Brassica napus during Cd stress (Xie et al., 2007). Genome-wide analysis of miRNA targets in Medicago truncatula under heavy-metal stress reported the varied response of plants under Cd and Hg exposure such as downregulation of miR166 and miR398. Besides these impacts the upregulation of miR393, miR171, miR319, and miR529 has also been analyzed (Zhou et al., 2008). The downregulation of miR159, miR160, miR319, miR396, and miR390 was also observed in M. truncatula during Al toxicity (Chen et al., 2012). Similarly, Hg-toxic legume seedlings showed the upregulation of miR167, miR172, miR169, miR164, miR395 and downregulation of miR396, miR390, and miR171 (Zhou et al., 2012).

28.6 MicroRNAs and oxidative stress Reactive oxygen species (ROS), such as superoxide radicals (SOR), hydrogen peroxide (H2O2), and hydroxyl radicals, are generated in cellular organelles, such as chloroplasts and mitochondria, in plant cells under normal conditions, but during stress conditions, the generation and accumulation of ROS lead to oxidative stress (Sharma et al., 2012). To cope with the oxidative stress, plant-defense system evolved the enzymatic and nonenzymatic antioxidant systems. In the enzymatic defense system, SODs, peroxidases (PODs), and catalases (CATs) are important enzymes, which scavenge the ROS species (Cruz de Carvalho, 2008). Plant Life under Changing Environment

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SODs are the most active enzymes, which convert highly unstable SOR into less toxic and stable products in the form of hydrogen peroxide, which is also detoxified by PODs and CATs. The expression of genes encoding SODs in plants has been well studied under various stress conditions. Sunkar et al. (2006) showed in their analysis that miR398 expression is downregulated transcriptionally due to oxidative burst, and this downregulation is important for post-transcriptional CSD1 and CSD2 mRNA accumulation and oxidative stress tolerance. Similarly, in rice seedlings, the analysis of seven oxidative stress
responsive miRNAs showed the upregulation of miR169, miR397, miR827, and miR1425 and downregulation of miR528 under oxidative stress (Li et al., 2011).

28.7 MicroRNAs and drought stress Under stress conditions, some genes activate and regulate the mechanism of posttranscription (Jones-Rhoades et al., 2006). miRNAs are key regulators in drought tolerance and they avert the stress by controlling and managing the expression of droughtresponsive genes (Covarrubias and Reyes, 2010). Different microassay-based methods have been applied to examine the drought-responsive miRNAs in various plant species such as Arabidopsis thaliana, O. sativa (Liu et al., 2008; Zhao et al., 2007), and Hordeum vulgare (Kantar et al., 2010). In the Arabidopsis seedlings, during the drought condition, the increased transcription of miR393, miR319, and miR397 has been observed (Sunkar and Zhu, 2004). Similar results were also found by Zhao et al. (2007) where the upregulation of drought-induced miRNA393 was observed in rice. Liu et al. (2008) also examined the stress-regulated miRNAs in Arabidopsis seedlings and analyzed the upregulation of miR157, miR167, miR168, miR171, miR408, miR393, and miR396. In Populus trichocarpa, a variation has been analyzed by Lu et al. (2008) in the transcription of miRNAs under drought stress and they reported the decreased accumulation of the miR1446a
e, miR1444a, miR1447, and miR1450 and moderately reduced accumulation of miRNAs such as miR1711a, miR482.2, miR530a, miR827, miR1445, and miR1448. Zhou et al. (2010) carried out genome-wide identification and analysis of drought-responsive miRNAs in O. sativa and showed the upregulation of 14 miRNAs and downregulation of 16 miRNAs. Two miRNAs, miR169g and miR393, are sturdily upregulated against drought stress in rice seedlings (Zhao et al., 2007). Zhou et al. (2010) also analyzed the miRNAs in droughtstressed rice seedlings from tillering to florescence stage and concluded that 16 miRNAs were remarkably upregulated in drought stress.

28.8 MicroRNAs and salt stress Salt stress is a severe abiotic stress for agriculture, and to alleviate its negative impact, plants evolved a substantial defense system including molecular network (Carillo et al., 2011). miRNA-guided post-transcriptional regulation plays an important role in the saltstress tolerance (Li et al., 2013). Several studies showed the relation between the plant development and adaptation toward stress. During the stress condition, the transcription of most of the miRNAs is altered, which are responsible for plant development and morphogenesis (Sunkar et al., 2007). These alterations induce the inhibition of plant Plant Life under Changing Environment

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development and morphogenesis by the cleavage of targeted mRNAs, which is responsible for the adaptation under stress conditions (Sunkar et al., 2007). Frazier et al. (2011) analyzed the aberrant expression of miRNA genes in 3-day old tobacco plants under salt stress and concluded that miR399, miR396, and miR172 were upregulated, which are responsible for phosphate homeostasis and leaf development, respectively. The overexpression of osa-miR393 has been seen in Arabidopsis exposed to high salinity, which may impart tolerance against salinity (Gao et al., 2011). Similarly, salt stress
responsive miRNAs were studied in radish (Raphanus sativus), which targeted the mRNAs related to signaling, ion-homeostasis and maintained the plant growth under stress conditions (Sun et al., 2015).

28.9 MicroRNAs and UV-B radiation Nowadays, the depletion of ozone layer has led to the increasing UV-B exposure on the Earth’s surface (McKenzie et al., 2003; Baroli et al., 2004; Jiao et al., 2005). Plants have photoreceptors to pick out red/far-red (phytochromes) radiations (Rizzini et al., 2011). UV-B induces several physiological processes in living organisms, but similarly, drought, salinity, high light intensities also produce pleiotropic impacts in plants by interacting with the endogenous developmental mechanisms (Baroli et al., 2004); therefore, to acclimatize to these kinds of stresses, plants have specific photoreceptors to monitor the UV-B radiation (Dunaeva and Adamska, 2001; Shao et al., 2006). By these photoreceptors, plants absorb the UV-B radiation and pass the information onto the nucleus, where the regulation of gene expression takes place (Kimura et al., 2003b; Jiao et al., 2005). Alteration in gene expression, in retort to UV-B radiation, produces a defense mechanism within plant cells (Kimura et al., 2003; Jiao et al., 2005). Jia et al. (2009) experimented with the UV-Bresponsive miRNAs in Populus tremula and examined a set of 24 UV-B stress
responsive miRNAs in which 13 upregulated and 11 downregulated

28.10 MicroRNAs and temperature stress Temperature is the foremost regulator of plant growth and development, but any variation in temperature, such as below or above the optimum condition, can cause stress in the plant cells and to alleviate these negative responses, plants cells generated a transduced complex signal in retort to that particular stress (You et al., 2014). In such signaling pathways the miRNAs are known to be involved, which regulate the expression of genes responsive to temperature stress (Ci et al., 2015). Ci et al. (2015) created a network between DNA methylation and miRNAs under temperature stress in Populus simonii and observed that five miRNA genes (MIR156i, MIR167h, MIR393a, MIR396e, and MIR396g) showed CG methylation and repression under cold stress. Moreover, on the contrary, hemi methylation at CNG and induction have been seen in heat stress, while in control condition, the miRNAs are unmethylated. However, heat-stressed miRNAs are less methylated in comparison to cold stress, which shows the increased expression of miRNAs in heat-stressed plants. Similarly, Lv et al. (2010) also identified 18 cold-responsive (4 C) miRNAs in rice, which are mostly downregulated, and also analyzed the heat-stress response in wheat Plant Life under Changing Environment

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seedlings and concluded that in between the 32 miRNA families, nine were conserved for heat response, and among these, miR172 downregulated and miR156, miR159, miR160, miR166, miR168, miR169, miR393, and miR827 were upregulated.

28.11 Conclusion and future outlook miRNAs regulate various biological and metabolic processes in plants, which may relate to several developmental aspects such as hormonal signaling, meristematic growth, organogenesis, leaf development, polarity, and regeneration. The whole transition in the plant from juvenile to adult and vegetative to flowering is regulated by

FIGURE 28.1 miRNA biogenesis and role of its key elements in growth and development of plants (Reinhart et al., 2002; Park et al., 2002). miRNA, MicroRNA.

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FIGURE 28.2 miRNA biogenesis and its expression pattern in plant cell under different abiotic stresses (Ding et al., 2013). miRNA, MicroRNA.

the miRNAs. Besides this, miRNAs are also the key regulators of stress-responsive genes. Abiotic stresses induce the unusual expression of various protein-coding genes in plants, but due to adaptive evolution, plants have evolved implausible capabilities to retort and adapt to stress conditions. Among these adaptations, cellular and molecular adaptation against abiotic stresses is acknowledged by the plant breeders and biotechnologists. In this context the research to understand the molecular response to abiotic stresses, such as metal stress, oxidative stress, salinity stress, drought stress, and UV-B stress, led to the identification of many differentially expressed miRNAs. The overexpression of many miRNAs also showed increased tolerance to abiotic stresses in model plant species. These results suggest that miRNAs, that can be used as potent candidates for genetic modification, impart abiotic stress tolerance to crop plants. Although the role of miRNAs in abiotic stress tolerance has been demonstrated, there is still a need for understanding the mechanism behind the role of different miRNAs in stress regulation (Figs. 28.1
28.2) (Table 28.1).

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TABLE 28.1 Upregulation and downregulation of miRNAs in different plants under several abiotic stresses. Abiotic stress

Plant

Upregulated miRNAs

Sulfate deprivation

Arabidopsis thaliana

miR395

Cd

Oryza sativa

miR528

Cd

Brassica napus

Cd and Hg

Medicago truncatula

Al Oxidative stress

Drought

Salinity

Downregulated miRNAs

References Ai et al. (2016)

miR162, miR166, miR171, miR390, miR168, and miR156

Ding et al. (2011)

miR393, miR171, miR156, and miR396

Xie et al. (2007)

miR166 and miR398

Zhou et al. (2008)

M. truncatula

miR159, miR160, miR319, miR396, and miR390

Chen et al. (2012)

A. thaliana

miR398

Sunkar et al. (2006)

miR528

Li et al. (2011)

miR393, miR171, miR319, and miR529

O. sativa

miR169, miR397, miR827, and miR1425

A. thaliana

miR393, miR319, and miR397

Sunkar and Zhu (2004)

A. thaliana

miR157, miR167, miR168, miR171, miR408, miR393, and miR396

Liu et al. (2008)

O. sativa

miR159, miR169, miR171, miR319, miR395, miR474, miR845, miR851, miR854, miR896, miR901, miR903, miR1026, miR1125

O. sativa

miR169g and miR393

O. sativa

miR159, miR169, miR171, miR319, miR395, miR474, miR845, miR851, miR854, miR896, miR901, miR903, miR1026, and miR1125

Nicotiana tobacum

miR399, miR396, and miR172

Frazier et al. (2011)

Arabidopsis

osa-miR393

Gao et al. (2011)

miR156, miR159, miR168, miR170, miR171, miR172, miR319, miR396, miR397, miR408, miR529, miR896, miR1030, miR1035, miR1050, miR1088, and miR1126

Zhou et al. (2008)

Zhao et al. (2007) miR156, miR159, miR168, miR170, miR171, miR172, miR319, miR396, miR397, miR408, miR529, miR896, miR1030, miR1035, miR1050, miR1088, and miR1126

Zhou et al. (2010)

(Continued)

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References

TABLE 28.1

(Continued)

Abiotic stress

Plant

Upregulated miRNAs

Downregulated miRNAs

References

UV-B radiation

Populus tremula

ath-miR156a, ath-miR160a, ath-miR164a; ptc-miR164f ptc, ath-miR165a, ath-miR166a; ptc-miR166p, osa-miR166l, ath-miR167a; ptc-miR167h ptc, ath-miR168a, osa-miR398b, osamiR408

ath-miR159a; ptc-miR159e, osamiR169e; ath-miR169a; ptcmiR169ab, ath-miR390a, osa-miR393b, mtr-miR395a, osa-miR399j, ptc-miR472a; ptc-miR472b

Jia et al. (2009)

MIR156i, MIR167h, MIR393a, MIR396e, and MIR396g

Ci et al. (2015)

miR172

Lv et al. (2010)

Temperature Populus simonii Triticum aestivum

miR156, miR159, miR160, miR166, miR168, miR169, miR393, and miR827

miRNA, MicroRNA.

References Achard, P., Herr, A., Baulcombe, D.C., Harberd, N.P., 2004. Modulation of floral development by a gibberellinregulated microRNA. Development 131 (14), 3357
3365. Agrawal, N., Dasaradhi, P.V.N., Mohmmed, A., Malhotra, P., Bhatnagar, R.K., Mukherjee, S.K., 2003. RNA interference: biology, mechanism, and applications. Microbiol. Mol. Biol. Rev. 67 (4), 657
685. Ai, Q., Liang, G., Zhang, H., Yu, D., 2016. Control of sulfate concentration by miR395-targeted APS genes in Arabidopsis thaliana. Plant Diversity 38 (2), 92
100. Aida, M., Ishida, T., Tasaka, M., 1999. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126, 1563
1570. Baroli, I., Gutman, B.L., Ledford, H.K., Shin, J.W., Chin, B.L., Havaux, M., et al., 2004. Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas. J. Biol. Chem. 279 (8), 6337
6344. Bartel, D.P., 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 (2), 281
297. Bonnet, E., Wuyts, J., Rouze´, P., Van de Peer, Y., 2004. Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proc. Natl. Acad. Sci. U.S.A. 101 (31), 11511
11516. Cai, Y., Yu, X., Hu, S., Yu, J., 2009. A brief review on the mechanisms of miRNA regulation. Genomics Proteomics Bioinf. 7 (4), 147
154. Carillo, P., Annunziata, M.G., Pontecorvo, G., Fuggi, A., Woodrow, P., 2011. Salinity stress and salt tolerance. In: Abiotic Stress in Plants—Mechanisms and Adaptations, IntechOpen press. Carrington, J.C., Ambros, V., 2003. Role of microRNAs in plant and animal development. Science 301 (5631), 336
338. Carthew, R.W., Sontheimer, E.J., 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136 (4), 642
655. Chen, X., 2005. MicroRNA biogenesis and function in plants. FEBS Lett. 579 (26), 5923
5931. Chen, X., 2008. MicroRNA metabolism in plants. RNA Interference. Springer Berlin Heidelberg, pp. 117
136. Chen, L., Wang, T., Zhao, M., Tian, Q., Zhang, W.H., 2012. Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235 (2), 375
386. Chinnusamy, V., Zhu, J., Zhu, J.K., 2007. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12 (10), 444
451. Cho, S.K., Ryu, M.Y., Shah, P., Poulsen, C.P., Yang, S.W., 2016. Post-translational regulation of miRNA pathway components, AGO1 and HYL1, in plants. Mol. Cells 39 (8), 581.

Plant Life under Changing Environment

730

28. Roles of microRNAs in plant development and stress tolerance

Ci, D., Song, Y., Tian, M., Zhang, D., 2015. Methylation of miRNA genes in the response to temperature stress in Populus simonii. Front. Plant Sci. 6, 921. Covarrubias, A.A., Reyes, J.L., 2010. Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs. Plant Cell Environ. 33 (4), 481
489. Cruz de Carvalho, M.H., 2008. Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal. Behav. 3 (3), 156
165. Ding, Y.F., Zhu, C., 2009. The role of microRNAs in copper and cadmium homeostasis. Biochem. Biophys. Res. Commun. 386 (1), 6
10. Ding, Y., Chen, Z., Zhu, C., 2011. Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J. Exp. Bot. 62, 3563
3573. Ding, Y., Tao, Y., Zhu, C., 2013. Emerging roles of microRNAs in the mediation of drought stress response in plants. J. Exp. Bot. 64 (11), 3077
3086. Dunaeva, M., Adamska, I., 2001. Identification of genes expressed in response to light stress in leaves of Arabidopsis thaliana using RNA differential display. FEBS J. 268 (21), 5521
5529. Eamens, A.L., Smith, N.A., Curtin, S.J., Wang, M.B., Waterhouse, P.M., 2009. The Arabidopsis thaliana doublestranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes. RNA 15 (12), 2219
2235. Eckardt, N.A., 2005. MicroRNAs regulate auxin homeostasis and plant development. Plant Cell 17 (5), 1335
1338. Emamverdian, A., Ding, Y., Mokhberdoran, F., Xie, Y., 2015. Heavy metal stress and some mechanisms of plant defense response. Sci. World J. 2015, 756120. Fang, Y., Spector, D.L., 2007. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol. 17 (9), 818
823. Felekkis, K., Touvana, E., Stefanou, C.H., Deltas, C., 2010. microRNAs: a newly described class of encoded molecules that play a role in health and disease. Hippokratia 14 (4), 236
240. Frazier, T.P., Sun, G., Burklew, C.E., Zhang, B., 2011. Salt and drought stresses induce the aberrant expression of microRNA genes in tobacco. Mol. Biotechnol. 49 (2), 159
165. Fu, X., Harberd, N.P., 2003. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421 (6924), 740
743. Gao, P., Bai, X., Yang, L., Lv, D., Pan, X., Li, Y., et al., 2011. osa-MIR393: a salinity-and alkaline stress-related microRNA gene. Mol. Biol. Rep. 38 (1), 237
242. Gielen, H., Remans, T., Vangronsveld, J., Cuypers, A., 2012. MicroRNAs in metal stress: specific roles or secondary responses? Int. J. Mol. Sci. 13 (12), 15826
15847. Grennan, A.K., 2008. Arabidopsis microRNAs. Plant Physiol. 146 (1), 3
4. Hong, Y., Jackson, S., 2015. Floral induction and flower formation—the role and potential applications of miRNAs. Plant Biotechnol. J. 13 (3), 282
292. Ho¨ck, J., Meister, G., 2008. The Argonaute protein family. Genome Biol. 9 (2), 210. Jia, X., Ren, L., Chen, Q.J., Li, R., Tang, G., 2009. UV-B-responsive microRNAs in Populus tremula. J. Plant Physiol. 166 (18), 2046
2057. Jiao, Y., Ma, L., Strickland, E., Deng, X.W., 2005. Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell 17 (12), 3239
3256. Jones-Rhoades, M.W., Bartel, D.P., 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14 (6), 787
799. Jones-Rhoades, M.W., Bartel, D.P., Bartel, B., 2006. MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19
53. Kantar, M., Unver, T., Budak, H., 2010. Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct. Integr. Genomics 10 (4), 493
507. Khraiwesh, B., Zhu, J.K., Zhu, J., 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta, Gene Regul. Mech. 1819 (2), 137
148. Kidner, C.A., Martienssen, R.A., 2004. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428 (6978), 81
84. Kim, V.N., Nam, J.W., 2006. Genomics of microRNA. Trends Genet. 22 (3), 165
173.

Plant Life under Changing Environment

References

731

Kim, Y.K., Yu, J., Han, T.S., Park, S.Y., Namkoong, B., Kim, D.H., et al., 2009. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic acids res 37 (5), 1672
1681. Kimura, M., Yamamoto, Y., Seki, M., Sakurai, T., Sato, M., et al., 2003b. Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem. Photobiol. 77, 226
233. Krogan, N.T., Hogan, K., Long, J.A., 2012. APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139 (22), 4180
4190. Leung, A.K., Sharp, P.A., 2010. MicroRNA functions in stress responses. Mol. Cell 40 (2), 205
215. Li, T., Li, H., Zhang, Y.X., Liu, J.Y., 2011. Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res. 39 (7), 2821
2833. Li, B., Duan, H., Li, J., Deng, X.W., Yin, W., Xia, X., 2013. Global identification of miRNAs and targets in Populus euphratica under salt stress. Plant Mol. Biol. 81 (6), 525
539. Liu, H.H., Tian, X., Li, Y.J., Wu, C.A., Zheng, C.C., 2008. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14 (5), 836
843. Llave, C., Xie, Z., Kasschau, K.D., Carrington, J.C., 2002. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 1053
1056. Lu, C., Fedoroff, N., 2000. A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12 (12), 2351
2365. Lu, S., Sun, Y.H., Chiang, V.L., 2008. Stress-responsive microRNAs in Populus. Plant J. 55 (1), 131
151. Lv, D.K., Bai, X., Li, Y., Ding, X.D., Ge, Y., Cai, H., et al., 2010. Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459 (1), 39
47. MacFarlane, L.A., Murphy, P.R., 2010. MicroRNA: biogenesis, function and role in cancer. Curr. Genomics 11 (7), 537
561. McConnell, J.R., Emery, J., Eshed, Y., Bao, N., Bowman, J., Barton, M.K., 2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411 (6838), 709
713. McKenzie, R.L., Bjo¨rn, L.O., Bais, A., Ilyasd, M., 2003. Changes in biologically active ultraviolet radiation reaching the Earth’s surface. Photochem. Photobiol. Sci. 2 (1), 5
15. Merelo, P., Ram, H., Caggiano, M.P., Ohno, C., Ott, F., Straub, D., et al., 2016. Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity. Proc. Natl. Acad. Sci. U.S.A. 113 (42), 11973
11978. Mette, M.F., Aufsatz, W., van der Winden, J., Matzke, M.A., Matzke, A.J., 2000. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 19, 5194
5201. Olena, A.F., Patton, J.G., 2010. Genomic organization of microRNAs. J. Cell. Physiol. 222 (3), 540
545. Park, W., Li, J., Song, R., Messing, J., Chen, X., 2002. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12 (17), 1484
1495. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., Bartel, D.P., 2002. MicroRNAs in plants. Genes Dev. 16 (13), 1616
1626. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., Bartel, D.P., 2002. Prediction of plant microRNA targets. Cell 110 (4), 513
520. Rizzini, L., Favory, J.J., Cloix, C., Faggionato, D., O’Hara, A., Kaiserli, E., et al., 2011. Perception of UV-B by the Arabidopsis UVR8 protein. Science 332 (6025), 103
106. Schauer, S.E., Jacobsen, S.E., Meinke, D.W., Ray, A., 2002. DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci. 7 (11), 487
491. Schwarz, D.S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., Zamore, P.D., 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell. 115 (2), 199
208. Shabalina, S.A., Koonin, E.V., 2008. Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. 23 (10), 578
587. Shao, N., Vallon, O., Dent, R., Niyogi, K.K., Beck, C.F., 2006. Defects in the cytochrome b6/f complex prevent light-induced expression of nuclear genes involved in chlorophyll biosynthesis. Plant Physiol. 141 (3), 1128
1137. Sharma, P., Jha, A.B., Dubey, R.S., Pessarakli, M., 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot. 2012, 217037.

Plant Life under Changing Environment

732

28. Roles of microRNAs in plant development and stress tolerance

Shivaraj, S.M., Singh, A., 2016. Sequence variation in Brassica AP2 and analysis of interaction of AP2-miR172 regulatory module. Plant Cell, Tissue Organ Cult. 125, 191
206. Shivaraj, S.M., Dhakate, P., Mayee, P., Negi, M.S., Singh, A., 2014. Natural genetic variation in MIR172 isolated from Brassica species. Biol. Plant. 58, 627
640. Shivaraj, S.M., Jain, A., Singh, A., 2018. Highly preserved roles of Brassica MIR172 in polyploid Brassicas: ectopic expression of variants of Brassica MIR172 accelerates floral transition. Mol. Genet. Genomics 293, 1121
1138. Shriram, V., Kumar, V., Devarumath, R.M., Khare, T.S., Wani, S.H., 2016. MicroRNAs as potential targets for abiotic stress tolerance in plants. Front. Plant Sci. 7, 817. Sun, X., Xu, L., Wang, Y., Yu, R., Zhu, X., Luo, X., et al., 2015. ). Identification of novel and salt-responsive miRNAs to explore miRNA-mediated regulatory network of salt stress response in radish (Raphanus sativus L.). BMC Genomics 16 (1), 197. Sunkar, R., Zhu, J.K., 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16, 2001
2019. Sunkar, R., Kapoor, A., Zhu, J.K., 2006. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18 (8), 2051
2065. Sunkar, R., Chinnusamy, V., Zhu, J., Zhu, J.K., 2007. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 12 (7), 301
309. Tang, G., Reinhart, B.J., Bartel, D.P., Zamore, P.D., 2003. A biochemical framework for RNA silencing in plants. Genes Dev. 17 (1), 49
63. Tripathi, A., Goswami, K., Sanan-Mishra, N., 2015. Role of bioinformatics in establishing microRNAs as modulators of abiotic stress responses: the new revolution. Front. Physiol. 6, 286. Available from: https://doi.org/ 10.3389/fphys.2015.00286. Wahid, F., Shehzad, A., Khan, T., Kim, Y.Y., 2010. MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochim. Biophys. Acta, Mol. Cell. Res. 1803 (11), 1231
1243. Wu, G., Park, M.Y., Conway, S.R., Wang, J.W., Weigel, D., Poethig, R.S., 2009. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138 (4), 750
759. Xie, F.L., Huang, S.Q., Guo, K., Xiang, A.L., Zhu, Y.Y., Nie, L., et al., 2007. Computational identification of novel microRNAs and targets in Brassica napus. FEBS Lett. 581 (7), 1464
1474. Yang, Q., Hua, J., Wang, L., Xu, B., Zhang, H., Ye, N., et al., 2013. MicroRNA and piRNA profiles in normal human testis detected by next generation sequencing. PloS one 8 (6), e66809. Yang, W., Chendrimada, T.P., Wang, Q., Higuchi, M., Seeburg, P.H., Shiekhattar, R., et al., 2006. Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nat. Struct. Mol. Biol. 13, 13
21. You, J., Zong, W., Hu, H.H., Li, X.H., Xiao, J.H., Xiong, L.Z., 2014. A STRESS-RESPONSIVE NAC1-regulated protein phosphatase gene rice protein phosphatase18 modulates drought and oxidative stress tolerance through abscisic acid-independent reactive oxygen species scavenging in rice. Plant Physiol. 166, 2100
2114. Available from: https://doi.org/10.1104/pp.114.251116. Yu, Y., Teng, Y., Liu, H., Reed, S.H., Waters, R., 2005. UV irradiation stimulates histone acetylation and chromatin remodeling at a repressed yeast locus. Proc. Natl. Acad. Sci. 102 (24), 8650
8655. Zhang, B., Pan, X., Cobb, G.P., Anderson, T.A., 2006. Plant microRNA: a small regulatory molecule with big impact. Dev. Biol. 289 (1), 3
16. Zhang, S., Zhou, J., Han, S., Yang, W., Li, W., Wei, H., et al., 2010. Four abiotic stress-induced miRNA families differentially regulated in the embryogenic and non-embryogenic callus tissues of Larix leptolepis. Biochem. Biophys. Res. Commun. 398 (3), 355
360. Zhang, J., Li, S., Li, L., Li, M., Guo, C., Yao, J., et al., 2015. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinf. 13 (1), 17
24. Zhao, B., Liang, R., Ge, L., Li, W., Xiao, H., Lin, H., et al., 2007. Identification of drought-induced microRNAs in rice. Biochem. Biophys. Res. Commun. 354 (2), 585
590. Zhou, Z.S., Huang, S.Q., Yang, Z.M., 2008. Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochem. Biophys. Res. Commun. 374 (3), 538
542. Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M., Luo, L., 2010. Genome-wide identification and analysis of droughtresponsive microRNAs in Oryza sativa. J. Exp. Bot. 61 (15), 4157
4168.

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Further reading

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Zhou, Z.S., Zeng, H.Q., Liu, Z.P., Yang, Z.M., 2012. Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ. 35 (1), 86
99.

Further reading Floris, M., Mahgoub, H., Lanet, E., Robaglia, C., Menand, B., 2009. Post-transcriptional regulation of gene expression in plants during abiotic stress. Int. J. Mol. Sci. 10 (7), 3168
3185. Mendoza-Soto, A.B., Sa´nchez, F., Herna´ndez, G., 2012. MicroRNAs as regulators in plant metal toxicity response. Front. Plant Sci. 3, 105. Zilberman, D., Cao, X., Jacobsen, S.E., 2003. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299, 716
719.

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C H A P T E R

29 Nitric oxide under abiotic stress conditions Juan C. Begara-Morales, Mounira Chaki, Raquel Valderrama, Capilla Mata-Pe´rez, Marı´a N. Padilla-Serrano and Juan B. Barroso Group of Biochemistry and Cell Signalling in Nitric Oxide, Department of Experimental Biology, Faculty of Experimental Sciences, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jae´n, Campus Universitario “Las Lagunillas” s/n, Jae´n, Spain

29.1 Introduction Nitric oxide (NO) is a gaseous biological messenger that modulates fundamental processes integral to plant biology via control of a wide range of physiological and stressresponse processes in plants (Mur et al., 2013; Domingos et al., 2015); for example, development (Begara-Morales et al., 2013), seed physiology (Albertos et al., 2015; Krasuska et al., 2015; Wang et al., 2015b; Krasuska et al., 2017), flowering (He et al., 2004), xylem vessel differentiation (Begara-Morales, 2018; Kawabe et al., 2018), stomatal movements (Wang et al., 2015a), and stress-related processes (Yu et al., 2014; Fancy et al., 2016). In animals, there is no debate regarding NO production, and it is clearly being well established that NO is produced by the action of a nitric oxide synthase (NOS) enzyme (Alderton et al., 2001). Conversely, NO production appears to be a much more complex mechanism in plants than in animals, involving several routes that can generate NO under different processes (Gupta et al., 2011; Astier et al., 2018). In this context, despite significant efforts to identify the main NO source(s), there are still a gap in the knowledge of what NO source(s) is(are) responsible for regulating NO-related signaling events in higher plants. Consequently, plant researchers have focused on NO-downstream signaling events to determine the mode of action of NO (Domingos et al., 2015). In this context, due to its liposoluble and radical nature, NO can diffuse across the membranes and react with

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biological molecules, such as proteins, lipids, and DNA, establishing the NO-downstream signaling events leading to regulate different processes. Traditionally, researchers have focused on the regulation of protein function by NO through protein posttranslational modifications (NO-PTMs), highlighting S-nitrosylation and tyrosine nitration. The former is a reversible protein modification consisting of the binding of NO to a thiol group within a reactive cysteine residue generating S-nitrosothiols (SNOs) (Hess et al., 2005), and the latter is considered an irreversible modification of tyrosine residues consisting of the addition of a NO2 group to its aromatic ring producing 3-nitrotyrosine (NO2-Tyr) (Gow et al., 2004; Radi, 2004). These NO-PTMs have been widely addressed in the literature, and as a result, it is generally accepted a fundamental function of SNOs in NO-related signaling events leading to face the environmental injuries (Yu et al., 2014; Begara-Morales et al., 2016a; Fancy et al., 2016) and a role of NO2-Tyr as a nitro-oxidative stress marker under these adverse situations (Corpas et al., 2007; Corpas and Barroso, 2013). Moreover, NO can also induce a transcriptional reprogramming leading to face the adverse environmental conditions. This statement is supported by the fact that different NO donors regulate the expression of stress-related genes (Polverari et al., 2003; Parani et al., 2004; Badri et al., 2008; Ferrarini et al., 2008; Ahlfors et al., 2009b; Begara-Morales et al., 2014b; Hussain et al., 2016; Singh et al., 2017; Imran et al., 2018). In this context, S-nitrosoglutathione (GSNO) is a major low-molecular SNO acting as a NO reservoir and a molecular signal to prompt the NO-dependent signaling events under stress-related processes in plants (Begara-Morales et al., 2018). In addition, nitro fatty acids (NO2-FAs) are NO-related molecules that can be formed by the reaction of NO with polyunsaturated FAs. In animals, it is well established that a key role of these NO2-FAs in physiological and pathological processes is mainly related to inflammatory processes (Deen et al., 2018). Interestingly, the occurrence of these molecules has been recently reported in plants (Mata-Perez et al., 2016b). Concretely, nitrolinolenic acid (NO2-Ln) has been suggested to have a crucial role in Arabidopsis development and environmental stresses (Mata-Perez et al., 2016b). Based on this background, this chapter will review the current insights about NO function during abiotic stress-related processes, with a special attention on NO production and function under these situations.

29.2 Nitric oxide sources under abiotic stress Although the occurrence of NO was first described in plants (Klepper, 1979), even before animals, the NO sources in plants are still under debate. In this regard the different routes with the potential capacity to generate NO can be grouped in two different pathways, the oxidative and the reductive one (Astier et al., 2018; Gupta et al., 2011). NOS-like activity and polyamines are the parts of oxidative routes, while nitrate reductase (NR), mitochondria, and plasma membrane associated NO can be classified as reductive routes (Fig. 29.1). Very recently, the amidoxime-reducing component (ARC) and NR enzymes have been proposed to generate NO from nitrites under hypoxic conditions (ChamizoAmpudia et al., 2016).

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FIGURE 29.1 NO production during plant response to abiotic stress. Different abiotic stress situations can modulate NO production in plants that ultimately mediate signaling processes leading to adaptive response to stress. It is generally accepted that NO is produced either in an oxidative or a reductive pathway. In this regard, NO can be synthesized from L-arginina by a NOS-like activity. Furthermore, arginine is the precursor of polyamines that can also induce the production of NO. On the other hand, NO can be produced from nitrite by NR and ARC have been also proposed to produce NO under specific conditions. More details in the text. ARC, Amidoximereducing component; NO, nitric oxide; NR, nitrate reductase.

29.2.1 Oxidative pathway 29.2.1.1 Nitric oxide like synthase In animals, NOS enzyme produces NO under physiological and pathological conditions, and therefore it is responsible for NO-signaling events. This NOS is responsible for the production of L-citrulline and NO using L-Arg as substrate. For this conversion, the presence of O2 and nicotinamide-adenine-dinucleotide phosphate using flavin adenine dinucleotide, flavin mononucleotide, tetrahydrobiopterin (BH4), calmoduline, and calcium as specific cofactors is necessary (Alderton et al., 2001). Nevertheless, there is still an intensive debate regarding the occurrence of a typical NOS in plants. In this context, some works have identified a NOS-like activity in higher plants, even using cofactors and inhibitors from animal NOS (Barroso et al., 1999; Corpas et al., 2009; Corpas and Barroso, 2014, 2017b; Santolini et al., 2017; Astier et al., 2018), but there is no clear evidence of a real NOS in plants (Jeandroz et al., 2016), even after sequencing several plant genomes. Some years ago, the Arabidopsis thaliana NOS 1 was described as a NOS enzyme (Guo et al., 2003). However, it was subsequently demonstrated that this protein is involved in NO biosynthesis, but it is not a real NOS, and, consequently, it was named A. thaliana NO-associated protein 1 (AtNOA1) (Moreau et al., 2008). atnoa1 mutants exhibit a reduced NO level in cells and is still used to analyze the role of NO endogenously produced. Interestingly, a NOS-like enzyme with an extra globin domain at the N-terminal has been recently described in the cyanobacteria Synechococcus PCC 7335 (Correa-Aragunde et al., 2018). Furthermore, a functional NOS was identified in the green alga Ostreococcus tauri (Foresi et al., 2011). These findings point that NOS enzyme could be lost early in evolution of plants or have evolved differently to animal NOS. Curiously, it has been suggested that NOS-like activity in plants could be regulated by different proteins that could work together to generate NO (Corpas and Barroso, 2017b). In this context the plant NOS structure would be totally different from animal NOS, and therefore all efforts to identify and

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purify a typical NOS in higher plants would be in vain. In any case, independently of its structure, the NOS-like activity has been reported to be involved in different physiological and stress-related processes (Chaki et al., 2011a, 2011b; Shi et al., 2014; Cai et al., 2015). In this sense the addition of an animal NOS inhibitor potentiates chilling stress in suspension cultured cells of Chorispora bungeana, suggesting a crucial role of this NO-generating enzyme during this stress response (Liu et al., 2010). Furthermore, a transgenic rice line overexpressing the neuronal rat NOS (nNOS) exhibits a higher tolerance to drought and salt stress than wild-type plants (Cai et al., 2015). The NOS-generated NO has also been proposed as relevant in response to elevated CO2 environments (Du et al., 2016). In this situation, NOS-mediated NO production can regulate the activity of NR, another crucial enzyme involved in NO generation in plants that is discussed in the next section. 29.2.1.2 Polyamines In addition to NOS-like activity, polyamines have been proposed to be able to produce NO from arginine (Tun et al., 2006) (Fig. 29.1). Chief polyamines (PAs) are putrescine (Put), spermidine (Spd), and spermine (Spm), which are synthesized from arginine (Wimalasekera et al., 2011). PAs are low-molecular compounds present ubiquitously in all living organisms that participate in the control of different pathways integral to plant biology (Wimalasekera et al., 2011). For example, PAs have been proposed to be involved in the regulation of the metabolism of apple embryos (Krasuska et al., 2017). Interestingly, pharmacological approaches using these compounds in Arabidopsis seedlings lead to a rapid production of NO (Tun et al., 2006). Although the biochemical mechanism by which NO is produced from PAs remains to be elucidated (Gupta et al., 2011), NO could be the signaling link between PAs and the physiological and stress-response processes mediated by PAs (Wimalasekera et al., 2011). In this sense, PAs appear to be involved in response to environmental changes (Wimalasekera et al., 2011). Spd triggered NO content in tomato seedlings leading to an adaptive response to chilling stress (Diao et al., 2016). A similar effect of Spd on antioxidant systems was observed during plant tolerance to aluminum stress (Nahar et al., 2017). Considering that aluminum stress induces NO production (Sahay and Gupta, 2017), NO could have a key role as mediator of Spd signaling leading to plant response to this stress.

29.2.2 Reductive pathway In addition to the oxidative route, NO can also be produced via a reductive pathway in which nitrites can be reduced to NO. This is probably the most characterized pathway of NO synthesis in higher plants. 29.2.2.1 Nonenzymatic The reduction of nitrites to NO is possible under special conditions such as acid environment and high nitrate concentrations. Although these particular situations are rare to be physiologically encountered, it has been described in apoplasts for instance (Bethke et al., 2004).

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29.2.2.2 Nitrate reductase Besides this, nonenzymatic production of NO, there are some proteins that enzymatically regulate NO production from nitrites. In this context the NR has emerged as a key enzyme involved in NO production that, in turn, regulates plant development and response to stress (Fu et al., 2018). NR is a limiting step in nitrogen assimilation pathway since it converts nitrate into nitrite with the participation of nicotinamide-adeninedinucleotide as cofactor. Interestingly, NR appears to be able to generate NO via the reduction of nitrite. Nevertheless, this reaction has a low efficiency in comparison to nitrate reduction capacity of NR (Dean and Harper, 1986; Gupta et al., 2011; Yamasaki and Sakihama, 2000). Apart from this, NR plays a crucial function in NO turnover (ChamizoAmpudia et al., 2017). In this sense, NO can be also produced from nitrite by the cooperation between NR and the molybdoenzyme ARC (Chamizo-Ampudia et al., 2016). Curiously, ARCs also produce NO in the membrane mitochondria under hypoxic conditions in humans (Sparacino-Watkins et al., 2014). NR is also able to positively regulate the NO elimination by the truncated hemoglobin THB1, and therefore it might be implicated in controlling NO homeostasis via regulation of the synthesis and elimination of NO (Chamizo-Ampudia et al., 2017). Independently of its mode of action, NR appears to have an important function in different physiological and adaptive responses to environmental stresses through NO generation (Fu et al., 2018; Mur et al., 2013). For instance, NRdependent NO generation are implicated in abiotic stresses (Zhao et al., 2009; Kolbert et al., 2010; Xie et al., 2013; Fu et al., 2018), stomatal actions (Hao et al., 2010; Desikan et al., 2002), or hormone metabolism (Kolbert and Erdei, 2008; Hao et al., 2010). 29.2.2.3 Other reductive pathways Alternative routes to NR have been proposed to generate NO from nitrite as a membrane-bound nitrite reductase (Ni:NOR), which was described in roots of Nicotiana tabacum (Stohr et al., 2001). In addition, mitochondria is a major source of NO under hypoxic conditions (Gupta et al., 2005; Planchet et al., 2005; Stoimenova et al., 2007; Gupta and Igamberdiev, 2011), in which NO could be produced with the participation of cytochrome c oxidase and/or reductase (Gupta and Igamberdiev, 2011).

29.3 Nitric oxide signaling under abiotic stress Environmental changes affect crops yield and production and therefore have a great economic impact. Chief among these adverse conditions are extreme temperature, salinity, drought, or heavy metals (HMs); the effects of most of them will be increased as consequence of the changing environment and global warming. In this regard, it has been predicted that at least 50% more production will be required to satisfy the necessity of the increasing population and to face the negative effects of the changing environment (Jaggard et al., 2010). In this context, understanding the signaling mechanisms leading to plant survival under adverse environmental conditions will be crucial to face the changing climate.

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It is perfectly described that abiotic stresses are generally characterized by the generation of reactive molecules as oxygen- and nitrogen-derived species (ROS and RNS), which mediate a nitro-oxidative stress (Corpas and Barroso, 2013). Prime ones among these molecules are hydrogen peroxide (H2O2) and nitric oxide (NO), which have a dual behavior depending on their cellular concentration: when they are present at low levels, they could act as molecular cues involved in plant response to stress; but at high levels, they can mediate oxidative and irreversible damages that ultimately lead to cell death. Interestingly, it is being established that the interplay between ROS- and RNS-related signaling pathways is crucial to trigger the plant response to abiotic stress (Lindermayr and Durner, 2015; Arora et al., 2016; Begara-Morales et al., 2016b; Lindermayr, 2017). As previously discussed, although significant efforts have been made to determine the main NO sources in plants, it is still under debate the NO source that regulates the physiological and stress-response processes in which NO has been involved. For this reason, researchers focused their attention on NO-downstream signaling to decipher the function of this biological messenger. This has allowed to determine that NO transmits its bioactivity via PTMs of proteins (NO-PTMs), highlighting tyrosine nitration and S-nitrosylation.

29.3.1 Salinity Salinity is a major abiotic stress with a negative impact on crops production and therefore has a great economic impact worldwide. Salt stress usually induces an osmotic stress that leads to poor water uptake (Khan et al., 2012). Furthermore, an excessive accumulation of Na 1 ions could result toxic for cells and induce electrolyte leakage and an ionic stress (Ahmad et al., 2014). NO and its related molecules appear to have a crucial role during salinity stress. In this context, NaCl induced a nitrosative stress in olive plants mediated by an increase in NOS like dependent NO levels along with an augment of S-nitrosylated and nitrated proteins (Valderrama et al., 2007). Salinity also induces NO accumulation in other plant species such as tomato (Manai et al., 2014), pea (Camejo et al., 2013; Begara-Morales et al., 2014a, 2015), orange (Tanou et al., 2009; Tanou et al., 2012), or tobacco plants (da Silva et al., 2017). Interestingly, the accumulation of NO could be responsible for S-nitrosylation of cysteine (Cys) 32 of ascorbate peroxidase (APX) in pea plants subjected to salt stress (Begara-Morales et al., 2014a). This modification increased its function removing H2O2 and, therefore, could have a crucial role alleviating the oxidative damage generated during salinity (Begara-Morales et al., 2014a). Subsequently, another work confirmed by genetic approaches that S-nitrosylation of Cys32 in Arabidopsis is crucial in the adaptive processes to oxidative stress (Yang et al., 2015). Besides the endogenous accumulation of NO in response to salinity, some works have carried out pharmacological approaches to analyze the involvement of NO in the tolerance processes during this environmental change. The exogenous application of sodium nitroprosside (SNP) enhanced the expression of ATPasa-H 1 pump and therefore enhancing plant tolerance to salinity (Zhao et al., 2004; Zhang et al., 2006), as well as seed germination in sunflower (David et al., 2010), Lupinus luteus (Kopyra and Gwozdz, 2003), and Suaeda salsa (Li et al., 2005). Arabidopsis transgenic lines deficient in NO production exhibit a lower rate of germination than wild type as consequence of an increased dormancy (Lozano-Juste and

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Leon, 2010). Exogenous SNP leads to a 40% of germination of these mutants in contrast to the 6% reached in the absence of this NO donor (Lozano-Juste and Leon, 2010). Interestingly, these mutants have lower germination efficiency than control plants as consequence of salt stress. It has been recently proposed that the enhancement of seed germination and plant growth by NO may depend on EIN3 protein in Arabidopsis under salt stress (Li et al., 2016). In this work, different Arabidopsis mutants with defective production of EIN3 protein and NO exhibited a lower germination rate than control plants subjected to salt conditions. This effect was also observed after the addition of 2-(4-carboxyphenyl)4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide as a NO scavenger to wild-type plants. In addition, under these conditions, NO was found to be crucial for EIN3 protein accumulation, and therefore it could control EIN3-downstream signaling events. A transgenic line overexpressing EIN3 protein behaved similarly to control, suggesting the crucial role of NO as regulator of EIN3 protein during the adaptive response of Arabidopsis plants to salinity (Li et al., 2016). On the other hand, the NO donor S-nitroso-N-acetylpenicillamine (SNAP) alleviates the oxidative damage generated by salinity conditions by improving the function of the antioxidant systems in chickpea (Ahmad et al., 2016). This highlights the control of ROS homeostasis by NO since the function of some antioxidant systems can be controlled by NO-PTMs (Arora et al., 2016; Begara-Morales et al., 2016b; GroB et al., 2013; Lindermayr and Durner, 2015). In this sense, NO regulates differentially the function of the ascorbateglutathione (Asa GSH) cycle during plant response to salt stress (Begara-Morales et al., 2014a, 2015) (Fig. 29.2). Tyrosine nitration promotes the inhibition of APX and monodehydroascorbate reductase (MDAR) enzymes, whereas S-nitrosylation enhances APX activity and inhibits MDAR function (Begara-Morales et al., 2014a, 2015). Surprisingly, these NO-PTMs do not modify the activity of the glutathione reductase that is involved in the

FIGURE 29.2 Regulation of ascorbate-glutathione cycle by NO during salinity stress. Salinity triggers a burst of NO and its derived molecules (RNS) that can regulate the function of the ascorbate-glutathione cycle (Asa GSH) by NO-related PTMs. In this regard, APX activity has a dual regulation by NO-PTMs, being enhanced by S-nitrosylation and inhibited by tyrosine nitration. Moreover, MDAR is inhibited by both modifications, whereas GR activity appears not to be affected by these modifications. APX, Ascorbate peroxidase; GR, glutathione reductase; MDAR, monodehydroascorbate reductase; NO, nitric oxide; PTMs, posttranslational modifications; RNS, reactive nitrogen species.

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recycling of the key antioxidant glutathione (GSH) (Begara-Morales et al., 2015). In addition, different components of the antioxidant systems, such as APX, iron-containing superoxide dismutase (Fe-SOD), MDAR, or glutaredoxin, have been identified as S-nitrosylated target under salt stress in citrus plants (Tanou et al., 2009; Tanou et al., 2012). These findings suggest that NO has an important function in the regulation of redox homeostasis during the adaptive response to salinity conditions.

29.3.2 Nitric oxide is a long-distance signal during wounding stress Plants usually have to face adverse conditions, such as hail, rain, wind, or herbivores, which can induce wounding (Corpas et al., 2011). This mechanical injury could cause both loss of nutrients and entry of pathogens, facilitating the subsequent infection (Savatin et al., 2014). For this reason, plants have evolved sophisticated defense mechanisms including physical barriers as well as hormones and different metabolites to protect themselves against mechanical injury (Savatin et al., 2014). Furthermore, NO has been involved as a molecular cue related to plant response to wounding stress. In this regard, wounding induces a rapid accumulation of NO in Arabidopsis plants, and this NO appears to be related to defense responses mediated by jasmonic acid (Huang et al., 2004). In pea leaves, wounding also induces NO level, probably as consequence of an increased NOS-like activity, along with the augment of total SNOs (Corpas et al., 2008). Moreover, wounding induces an early and transient NO generation at the site of the injury in pelargonium plants (Arasimowicz et al., 2009). Exogenous SNAP showed that NO slightly decreases O22 and increases H2O2 levels probably as consequence of the inhibition of catalase and APX enzymes (Arasimowicz et al., 2009). Conversely, exogenous SNP reduces cell death, O22 and H2O2 levels while increasing SOD and APX activities in Ipomoea batatas plants (Lin et al., 2011). This apparent discordance between the regulation of ROS and antioxidant systems by NO after wounding could be a consequence of the different species or NO donors used in each study. S-Nitrosoglutathione (GSNO) is crucial in the regulation of NO-dependent events and therefore is fundamental during the adaptive response to the abiotic stresses. In this context the metabolism of GSNO is crucial to understand NO bioactivity (Begara-Morales et al., 2018). In this regard, NOS-like and NR activities do not change, and therefore NO level is not altered after 4 hours of wounding in sunflower hypocotyls (Chaki et al., 2011a). However, a nitrosative stress is induced as a consequence of the accumulation of GSNO and total SNOs in sunflowers subjected to wounding injuries (Chaki et al., 2011a). Interestingly, GSNO appears to have a key signaling function that contributes to spread the wound signal via the vascular tissue (Espunya et al., 2012). This signal could be transmitted by vascular bundles since that the ability of the phloem to disseminate redox molecules such as several types of RNS has been recently proposed (Gaupels et al., 2017). In the same line, hypocotyl wounding in Cakile maritima L. induces a response in unwounded tissues suggesting that ROS and RNS could be involved in long-distance signals after mechanical injury (Houmani et al., 2018). On the other hand, wounding decreases S-nitrolyated while increasing nitrated proteins in extrafascicular phloem of Cucurbita maxima (Gaupels et al., 2016).

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29.3.3 Heat stress High-temperature (HT) stress has a high negative impact on plant growth. It negatively affects both vegetative and reproductive growth, being one of the abiotic stresses that have a greater impact on crop yield (Li et al., 2018a). Thus the global warming derived from the climate change will have a negative impact on agriculture and consequently economic losses. For this reason, to understand the processes used by plants to face HT will help to develop plants with an enhanced resistance to this stress (Li et al., 2018a), which could be used in breeding programs contributing to increase the food security. Plants sense HT and trigger a complex response mechanism involving expression of heat shock proteins, hormones, and signaling molecules such as ROS or calcium that mediates cellular responses leading to the adaptive response to the generated stress (Parankusam et al., 2017; Li et al., 2018a). In the last decade, NO has emerged as a pivotal player in thermotolerance acquisition in plants, working cooperatively with the rest of signaling molecules (Parankusam et al., 2017; Li et al., 2018a). In this sense, NO has been related to regulate gene expression, membrane integrity, seed dormancy, and osmolyte accumulation in plants subjected to heat conditions (Parankusam et al., 2017). Heat stress induces NO generation in alfalfa (Leshem et al., 1998) and tobacco (Gould et al., 2003). However, in pea plants (Corpas et al., 2008) and sunflower hypocotyls (Chaki et al., 2011b), which are subjected to heat stress, a decrease in NO levels was observed. These contradictory data suggest that HTs alter NO metabolism, but the response depends on the species, tissue, and stress conditions used (Corpas et al., 2011). Despite the decline in NO level and production in sunflower hypocotyls, there is an increase in total SNOs that mediate the accumulation of tyrosine nitration content (Chaki et al., 2011b). This NO-mediated modification of tyrosine residue negatively regulates the function of the ferredoxin-NADP reductase and anhydrase carbonic enzymes, which are proteins involved in the photosynthetic carbon assimilation pathway (Chaki et al., 2011b, 2013). This result confirms NO as a signal molecule with an important function in the regulation of photosynthesis process during heat stress response (Parankusam et al., 2017). One of the first genetic evidences showing the involvement of NO in plant thermotolerance was carried out using HOT5/GSNOR (Snitrosoglutathione reductase)-deficient mutant plants (Lee et al., 2008). These mutants accumulate more nitrate and nitroso species that lead to an increased sensitivity to heat stress. Conversely, different Arabidopsis mutants impaired in NO biosynthesis such as atnoa1 (for nitric oxide associated protein 1) and nia1nia2 (for NR-defective double mutant) exhibit a lower plant survival rate than wild-type plants following heat treatment (Xuan et al., 2010). Furthermore, a rescued line of atnoa1 presents a partially restored survival ratio (Xuan et al., 2010). In addition, exogenously applied NO donors SNP or SNAP improve plant survival after heat stress, suggesting that NO has a key role regulating plant response to heat stress. Calmoduline 3 (cam3) has been proposed to be heat induced and involved in HT responses in Arabidopsis (Liu et al., 2005; Zhang et al., 2009). Interestingly, in cam3 or cam3noa1 double mutants, the exogenously applied SNP does not enhance plant survival, suggesting that NO regulates AtCam3 in Arabidopsis plants subjected to heat stress (Xuan et al., 2010). Other evidences point toward cross talk between NO and H2O2 in heat conditions (Li et al., 2018a). In an elegant genetic approach using H2O2 and NOdefective mutants, Wang et al. (2014) proposed that H2O2 acts upstream NO in the heat shock pathway during thermotolerance of Arabidopsis plants. In addition, heat stress Plant Life under Changing Environment

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enhances NO production that, in turn, promotes proline accumulation and positively regulates the function of the antioxidant systems leading to a thermotolerance response in Vicia faba (Alamri et al., 2018). Interestingly, the occurrence of NO2-FAs has been recently described in plants (MataPerez et al., 2016b). Among them, the nitrolinolenic acid (NO2-Ln) is a NO donor (MataPerez et al., 2016a) that may participate in plant response to abiotic stress (Mata-Perez et al., 2016b). In this regard a RNA-seq analysis revealed that NO2-Ln is a regulator of the heat shock proteins and the chaperone network, suggesting a key role of these signaling molecules during plant acclimation to heat stress (Mata-Perez et al., 2016b).

29.3.4 Low temperatures Low-temperature (LT) stress can affect essential processes such as mineral and water uptake, photosynthesis, or ion homeostasis along with changes in cell membranes and induction of ROS (Selvarajan et al., 2018). Consequently, LT is an environmental stress that can also affect plant growth and therefore crop productivity. This stress can modulate gene expression that is potentially implicated on cold acclimation (Selvarajan et al., 2018). In addition, LT has also an impact on NO metabolism (Corpas et al., 2008; Airaki et al., 2012; Sehrawat et al., 2013). In pea plants, LT stress increases NOS like mediated NO production with an associated increase of total SNOs and nitrated proteins, generating a nitrosative stress (Corpas et al., 2008). In pepper leaves subjected to LT stress for 24 hours, there is an imbalance in ROS and RNS metabolism leading to lipid peroxidation and tyrosine nitration of proteins and consequently inducing a nitrosative stress (Airaki et al., 2012). LT and chilling stress accumulated ROS-related molecules that induce an oxidative stress and therefore reducing cell viability in C. bungeana (Liu et al., 2010). This oxidative stress was significantly improved by a NO donor and aggravated by molecules that remove NO, suggesting a key role of NOS like generated NO in regulating plant response to this environmental condition. The protective effect of NO was probably the consequence of the reduction of ROS levels via control of the key antioxidant systems (Liu et al., 2010). In a similar way the addition of SNP decreased the negative consequences produced by cold stress on wheat seedlings by both reducing ROS level and stimulating antioxidant systems (Esim et al., 2014). In addition, in an elegant work using deficient and overexpressing mutants, a crucial role of the AtNOA1 gene in cucumber tolerance to chilling stress was proposed (Liu et al., 2016). Regarding the potential NO signaling in plant response to LT, several protein targets of S-nitrosylation have been identified (Abat and Deswal, 2009; Sehrawat et al., 2013 Puyaubert et al., 2014). The S-nitrosylation of Fe-SOD enhances its function and consequently protects against the negative effects of cold stress on Brassica juncea (Sehrawat et al., 2013). In addition, 20 differentially S-nitrosylated proteins were identified in Arabidopsis under cold conditions (Puyaubert et al., 2014). These S-nitrosylated proteins are a good starting point to analyze the effect of NO on regulating plant tolerance to LT stress.

29.3.5 Heavy metals Heavy metals (HM) levels are rapidly increasing as consequence of human activities, resulting in a global environmental concern. HM can be accumulated in soil, and therefore Plant Life under Changing Environment

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they can enter food chain and induce damages not only in plants, but also in animals and humans (Gall et al., 2015). As immobile living beings, plants exhibit a basal tolerance to HMs. However, they may result in toxic when reach high concentrations in soil and induce cellular damages that ultimately affect plant growth and development (Kramer and Clemens, 2005). NO, as a crucial signaling molecule that transduces the stress signal, has been involved in plant response to HM accumulation (Barroso et al., 2006; He et al., 2014; Sahay and Gupta, 2017). In this context, when the HM stress is perceived, NO generation can regulate gene expression and mediate NO-PTMs leading to a defensive response against this adverse situation (Sahay and Gupta, 2017). NO level, along with GSNO and its catabolic enzyme GSNOR, was markedly reduced in collenchyma cells in pea plants grown at toxic concentrations of cadmium (50 μM Cd) (Barroso et al., 2006). This NO reduction could be a consequence of the inactivation of the NOS-like activity due to the reduction of calcium levels provoked by Cd stress (Rodriguez-Serrano et al., 2009). NO appears to have a function in HM stress due to its capacity for regulating ROS level through control of the function of the antioxidant systems (Procha´zkova´ et al., 2014). In this sense, lead (Pb) stress induces NO production that, in turn, negatively regulates catalase activity in Arabidopsis peroxisomes (Corpas and Barroso, 2017a). Furthermore, catalase and glycolate oxidase are inhibited by S-nitrosylation in response to Cd stress (OrtegaGalisteo et al., 2012). Consequently, the authors proposed that NO might be involved in the regulation of H2O2 levels and therefore regulating redox homeostasis in peroxisomes (Ortega-Galisteo et al., 2012). Exogenous spermidine induces the antioxidant machinery under aluminum stress in Vigna radiata (Nahar et al., 2017). Spermidine belongs to polyamines family that is able to induce NO production in plants (Tun et al., 2006). Unfortunately, in this work, NO levels were not determined to verify the fact whether it is responsible for enhancing the antioxidant machinery leading to aluminum tolerance in these plants (Nahar et al., 2017). In this context the modulation of ROS metabolism by NO has been related to copper (Cu) tolerance in Arabidopsis plants (Peto et al., 2013). Interestingly, 5 μM Cu compromises cell viability in NO overproducing mutants, nox1 and atgsnor1 3 compared to wild-type plants. However, higher concentrations of Cu (25 and 50 μM) enhanced the viability of these mutants while compromising the viability of NO-defective mutants, nia1nia2 (Peto et al., 2013). These results were also corroborated by using NO donors and scavengers, suggesting that NO can enhance the sensitivity or tolerance to Cu depending on the strength of the stress (Peto et al., 2013).

29.3.6 Drought Climate change and global warming will bring a multitude of atmospheric changes that could impact on crops growth and productivity. In last years, as consequence of increasing gas emission and temperatures, scientists have related climate change to the increase of arid areas, showing a real concern about water deficit around the world. This could be a serious problem because drought can lead to crop damage and therefore affecting the farmers and communities that depend on agriculture. For this reason, understanding the tolerance mechanisms to drought stress could help in breeding programs leading to crops with and improved tolerance to water deficit. In this line, NO is a fundamental molecule Plant Life under Changing Environment

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that can orchestrate plant defense against drought (Santisree et al., 2015). The role of NO has been related to its capacity to regulate stomatal movement and closure, but it can also modulate other crucial plant processes as photosynthesis or seed germination (reviewed in Santisree et al., 2015). A rice transgenic line overexpressing rat neuronal NOS, with enhanced levels of NO, exhibits tolerance to drought stress (Cai et al., 2015). In this mutant line, there is less accumulation of ROS-related molecules while increasing proline, antioxidant funcion, and drought-related gene expression (Cai et al., 2015). A similar strategy was employed to show an improved tolerance to drought in Arabidopsis (Shi et al., 2014). These results suggest a key role of NOS like generated NO in plant adaptation to water deficit. Conversely, the overexpression of nonsymbiotic hemoglobin gene HvHb1, which exhibits lower NO levels than wild type, increases barley tolerance to drought stress (Montilla-Bascon et al., 2017). Moreover, drought stress induces a nitro-oxidative stress in roots and leaves of Lotus japonicus, increasing the level of nitrated proteins related to crucial processes mainly involved in plant defense (Signorelli et al., 2015; Signorelli et al., 2018). Furthermore, the exogenous SNP leads to water deficit tolerance in Crambe abyssinica plants (Batista et al., 2018). Collectively, most of studies on NO-mediated signaling under drought stress are descriptive, so that a deeper characterization of NO signaling at molecular level is required. For instance, the identification of protein candidates of S-nitrosylation under drought stress and the analysis of this modification on their function and structure could be a good starting point to moving forward in this field.

29.3.7 Nitric oxide and ozone stress Ozone (O3) is crucial for the life on the Earth. However, it can exert a dual function depending on its localization: in the stratosphere, O3 protects from the sun’s harmful ultraviolet radiation, whereas in troposphere, it can induce oxidative stress that ultimately causes cell death (Langerbartels et al., 2002; Kangasjarvi et al., 2005; Cho et al., 2011) and consequently being injurious for human health, vegetation and crop productivity (Cho et al., 2011; Fares et al., 2013). O3 enters the leaves through the stoma and its effect depends on concentration, exposure time, and crop and cultivar analyzed (Corpas et al., 2011; Cho et al., 2011; Vainonen and Kangasjarvi, 2015). At low concentrations, O3 alters photosynthesis and growth, whereas high concentrations induce cell death and therefore compromising plant survival (Corpas et al., 2011). Once inside the cells, O3 can be converted into several ROS and consequently induces an oxidative stress that can compromise plant survival (Cho et al., 2011), since that O3 is able to modulate protein function and gene expression (Vainonen and Kangasjarvi, 2015). As an air pollutant, O3 is increasing as consequence of industrialization. In this context, its accumulation is being considered one of the major abiotic stresses affecting crop productivity and therefore global food security (Cho et al., 2011). Within the O3-triggered signaling events, NO has emerged as a key player (Corpas et al., 2011; Vainonen and Kangasjarvi, 2015). O3 stress induces endogenous production of NO that ultimately has been proposed to increase the antioxidant systems function and therefore reducing H2O2, malondialdehyde (MDA), and electrolyte leakage in wheat plants (Li et al., 2018b). Consequently, NO appears to have a fundamental function during wheat tolerance to ozone accumulation (Li et al., 2018b). Moreover, NO may have a role in Plant Life under Changing Environment

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ozone-mediated signaling by modifying the levels of salicylic acid (SA) and ethylene along with changes in gene expression (Ahlfors et al., 2009a, 2009c). NO-signaling events are usually mediated by S-nitrosylation. In this context an S-nitrosoproteomic study was performed under acute ozone stress in poplar (Vanzo et al., 2014). In total, 172 endogenously S-nitrosylated proteins related to primary and secondary metabolism were identified by a combination of biotin switch and label-free liquid chromatography-tandem mass spectrometry analysis (Vanzo et al., 2014). Plants were exposure to an intense O3 stress for 1 hour, being enough to induce changes in the S-nitrosylation status of 32 proteins. Most of these proteins were denitrosylated after O3 treatment. For instance, the activity of phenylalanine ammonia-lyase, an important enzyme in phenylpropanoid biosynthesis pathway, is enhanced after the denitrosylation derived from O3 stress (Vanzo et al., 2014).

29.4 Conclusion and perspectives Environmental changes derived from climate change will have a great impact on crop growth and productivity and consequently will constitute a serious problem for food security in the forthcoming decades. For this reason, understanding the signaling mechanisms leading to plant adaptation to specific adverse conditions will help in the design of strategies to obtain crops more tolerant to the adverse environmental conditions. In this scenario, several signaling molecules belonging to ROS and RNS have been proposed as fundamental mediators of signaling events during tolerance processes. In this context, NO has emerged as a key bioactive molecule that governs a multitude of physiological processes and stress response in higher plants. Despite its crucial role as signaling molecule, the specific sources of NO synthesis in plants are still under debate. Although a NOS-like activity has been widely described, a typical NOS has not been yet identified in plants. This is probably because NOS-like activity in plants could be produced by a protein with a different structure relative to the animal one. Recently, the idea that different proteins can act together to produce NO in a NOS-like manner has been proposed. Efforts have to be made to confirm this hypothesis and finally resolve this problem regarding NO synthesis in plants. In addition, most of the studies analyzing the role of NO during plant response to stress have been performed under laboratory conditions, and only one type of stress has been analyzed. However, crops are not only exposed to a single environmental insult in the field. In this context the analysis of the effect of at least two environmental insults at the same time will better reflect the field conditions. Independently of its mode of production, NO usually transmits its bioactivity regulating gene expression and mainly modulating protein function via PTMs such as S-nitrosylation and tyrosine nitration. In this line, there are a high number of proteins that are target of NO under a wide variety of environmental stresses, but there is still insufficient information on the in vivo function of these modifications, and therefore significant efforts have to be made to moving forward in this field. A deeper characterization of these NO targets at molecular level during plant response to stress will be essential to increase our understanding in plant adaptation to stress and consequently to facilitate the use of NO in Plant Life under Changing Environment

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biotechnological strategies that could be applied in breeding programs to improve crop tolerance to abiotic stresses.

Acknowledgments JCBM wishes to thank the Ministry of Economy and Competitiveness (Spain) for postdoctoral research funding within the Juan de la Cierva-Incorporacio´n program (IJCI-2015-23438). The work in our lab is supported by the ERDF grants cofinanced by the Ministry of Economy and Competitiveness (projects BIO2015 66390-P) and the Junta de Andalucı´a (group BIO286) in Spain.

References Abat, J.K., Deswal, R., 2009. Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics. 9, 4368 4380. Ahlfors, R., Brosche, M., Kangasjarvi, J., 2009a. Ozone and nitric oxide interaction in Arabidopsis thaliana: a role for ethylene? Plant Signaling Behav. 4, 878 879. Ahlfors, R., Brosche, M., Kollist, H., Kangasjarvi, J., 2009b. Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J. 58, 1 12. Ahlfors, R., Brosche´, M., Kollist, H., Kangasjarvi, J., 2009c. Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J. 58, 1 12. Ahmad, P., Ozturk, M., Sharma, S., Gucel, S., 2014. Effect of sodium carbonate-induced salinity alkalinity on some key osmoprotectants, protein profile, antioxidant enzymes, and lipid peroxidation in two mulberry (Morus alba L.) cultivars. J. Plant Interact. 9, 460 467. Ahmad, P., Abdel Latef, A.A., Hashem, A., Abd Allah, E.F., Gucel, S., Tran, L.S., 2016. Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front. Plant Sci. 7, 347. Airaki, M., Leterrier, M., Mateos, R.M., Valderrama, R., Chaki, M., Barroso, J.B., et al., 2012. Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ. 35, 281 295. Alamri, S.A., Siddiqui, M.H., Al-Khaishany, M.Y., Khan, M.N., Ali, H.M., Alakeel, K.A., 2018. Nitric oxidemediated cross-talk of proline and heat shock proteins induce thermotolerance in Vicia faba L. Environ. Exp. Bot. Available from: https://doi.org/10.1016/j.envexpbot.2018.1006.1012. Albertos, P., Romero-Puertas, M.C., Tatematsu, K., Mateos, I., Sa´nchez-Vicente, I., Nambara, E., et al., 2015. S-Nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat. Commun. 6, 8669. Alderton, W.K., Cooper, C.H., Knowles, R., 2001. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357, 593 615. Arasimowicz, M., Floryszak-Wieczorek, J., Milczarek, G., Jelonek, T., 2009. Nitric oxide, induced by wounding, mediates redox regulation in pelargonium leaves. Plant Biol. 11, 650 663. Arora, D., Jain, P., Singh, N., Kaur, H., Bhatla, S.C., 2016. Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants. Free Radical Res. 50, 291 303. Astier, J., Gross, I., Durner, J., 2018. Nitric oxide production in plants: an update. J. Exp. Bot. 69, 3401 3411. Badri, D.V., Loyola-Vargas, V.M., Du, J., Stermitz, F.R., Broeckling, C.D., Iglesias-Andreu, L., et al., 2008. Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytol. 179, 209 223. Barroso, J.B., Corpas, F.J., Carreras, A., Sandalio, L.M., Valderrama, R., Palma, J.M., et al., 1999. Localization of nitric-oxide synthase in plant peroxisomes. J. Biol. Chem. 274, 36729 36733. Barroso, J.B., Corpas, F.J., Carreras, A., Rodrı´guez-Serrano, M., Esteban, F.J., Ferna´ndez-Ocan˜a, A., et al., 2006. Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J. Exp. Bot. 57, 1785 1793. Batista, P.F., Costa, A.C., Muller, C., Silva-Filho, R.O., Barbosa da Silva, F., Merchant, A., et al., 2018. Nitric oxide mitigates the effect of water deficit in Crambe abyssinica. Plant. Physiol. Biochem. 129, 310 322.

Plant Life under Changing Environment

References

749

Begara-Morales, J.C., 2018. GSNOR regulates VND7-mediated xylem vessel cell differentiation. Plant Cell Physiol. 59, 5 7. Begara-Morales, J.C., Chaki, M., Sa´nchez-Calvo, B., Mata-Pe´rez, C., Leterrier, M., Palma, J.M., et al., 2013. Protein tyrosine nitration in pea roots during development and senescence. J. Exp. Bot. 64, 1121 1134. Begara-Morales, J.C., Sa´nchez-Calvo, B., Chaki, M., Valderrama, R., Mata-Pe´rez, C., Lo´pez-Jaramillo, J., et al., 2014a. Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J. Exp. Bot. 65, 527 538. Begara-Morales, J.C., Sa´nchez-Calvo, B., Luque, F., Leyva-Pe´rez, M.O., Leterrier, M., Corpas, F.J., et al., 2014b. Differential transcriptomic analysis by RNA-seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol. 55, 1080 1095. Begara-Morales, J.C., Sa´nchez-Calvo, B., Chaki, M., Mata-Pe´rez, C., Valderrama, R., Padilla, M.N., et al., 2015. Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J. Exp. Bot. 66, 5983 5996. Begara-Morales, J.C., Sanchez-Calvo, B., Chaki, M., Valderrama, R., Mata-Perez, C., Corpas, F.J., et al., 2016a. Protein S-nitrosylation and S-glutathionylation as regulators of redox homeostasis during abiotic stress response. In: Gupta, D.K., et al., (Eds.), Redox State as a Central Regulator of Plant-Cell Stress Responses. Springer, pp. 365 386. Begara-Morales, J.C., Sa´nchez-Calvo, B., Chaki, M., Valderrama, R., Mata-Pe´rez, C., Padilla, M.N., et al., 2016b. Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front. Plant Sci. 7, 152. Begara-Morales, J.C., Chaki, M., Valderrama, R., Sanchez-Calvo, B., Mata-Perez, C., Padilla, M.N., et al., 2018. Nitric oxide buffering and conditional nitric oxide release in stress response. J. Exp. Bot. 69, 3425 3438. Bethke, P.C., Badger, M.R., Jones, R.L., 2004. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16, 332 341. Cai, W., Liu, W., Wang, W.-S., Fu, Z.-W., Han, T.-T., Lu, Y.-T., 2015. Overexpression of rat neurons nitric oxide synthase in rice enhances drought and salt tolerance. PLoS One 10, e0131599. Camejo, D., Romero-Puertas, M., Rodriguez-Serrano, M., Sandalio, L.M., La´zaro, J.J., Jime´nez, A., et al., 2013. Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J. Proteomics 79, 87 99. Chaki, M., Valderrama, R., Ferna´ndez-Ocan˜a, A.M., Carreras, A., Go´mez-Rodı´guez, M.V., Pedrajas, J.R., et al., 2011a. Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J. Exp. Bot. 62, 1803 1813. Chaki, M., Valderrama, R., Ferna´ndez-Ocan˜a, A.M., Carreras, A., Go´mez-Rodrı´guez, M.V., Lo´pez-Jaramillo, J., et al., 2011b. High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ. 34, 1803 1818. Chaki, M., Carreras, A., Lo´pez-Jaramillo, J., Begara-Morales, J.C., Sa´nchez-Calvo, B., Valderrama, R., et al., 2013. Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (β-CA) activity under high temperature stress. Nitric Oxide 29, 30 33. Chamizo-Ampudia, A., Sanz-Luque, E., Llamas, A., Ocan˜a-Calahorro, F., Mariscal, V., Carreras, A., et al., 2016. A dual system formed by the ARC and NR molybdoenzymes mediates nitrite-dependent NO production in Chlamydomonas. Plant Cell Environ. 39, 2097 2107. Chamizo-Ampudia, A., Sanz-Luque, E., Llamas, A., Galvan, A., Fernandez, E., 2017. Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci. 22, 163 174. Cho, K., Tiwari, S., Agrawal, S.B., Torres, N.L., Agrawal, M., Sarkar, A., et al., 2011. Tropospheric ozone and plants: absorption, responses, and consequences. Rev. Environ. Contam. Toxicol. 212, 61 111. Corpas, F.J., Barroso, J.B., 2013. Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol. 199, 633 635. Corpas, F.J., Barroso, J.B., 2014. Peroxisomal plant nitric oxide synthase (NOS) protein is imported by peroxisomal targeting signal type 2 (PTS2) in a process that depends on the cytosolic receptor PEX7 and calmodulin. FEBS Lett. 588, 2049 2054. Corpas, F.J., Barroso, J.B., 2017a. Lead-induced stress, which triggers the production of nitric oxide (NO) and superoxide anion (O2(2)) in Arabidopsis peroxisomes, affects catalase activity. Nitric Oxide 68, 103 110. Corpas, F.J., Barroso, J.B., 2017b. Nitric oxide synthase-like activity in higher plants. Nitric Oxide 68, 5 6.

Plant Life under Changing Environment

750

29. Nitric oxide under abiotic stress conditions

Corpas, F.J., Luis, A., Barroso, J.B., 2007. Need of biomarkers of nitrosative stress in plants. Trends Plant Sci. 12, 436 438. Corpas, F.J., Chaki, M., Ferna´ndez-Ocan˜a, A., Valderrama, R., Palma, J.M., Carreras, A., et al., 2008. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol. 49, 1711 1722. Corpas, F.J., Palma, J.M., Del Rı´o, L.A., Barroso, J.B., 2009. Evidence supporting the existence of L-arginine-dependent nitric oxide synthase activity in plants. New Phytol. 184, 9 14. Corpas, F.J., Leterrier, M., Valderrama, R., Airaki, M., Chaki, M., Palma, J.M., et al., 2011. Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci. 181, 604 611. Correa-Aragunde, N., Foresi, N., Del Castello, F., Lamattina, L., 2018. A singular nitric oxide synthase with a globin domain found in Synechococcus PCC 7335 mobilizes N from arginine to nitrate. Sci. Rep. 8, 12505. da Silva, C.J., Batista Fontes, E.P., Modolo, L.V., 2017. Salinity-induced accumulation of endogenous H2S and NO is associated with modulation of the antioxidant and redox defense systems in Nicotiana tabacum L. cv. Havana. Plant Sci. 256, 148 159. David, A., Yadav, S., Bhatla, S.C., 2010. Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiol. Plant. 140, 342 354. Dean, J.V., Harper, J.E., 1986. Nitric oxide and nitrous oxide production by soybean and winged bean during the in vivo nitrate reductase assay. Plant Physiol. 82, 718 723. Deen, A.J., Sihvola, V., Ha¨rkonen, J., Patinen, T., Adinolfi, S., Levonen, A.-L., 2018. Regulation of stress signaling pathways by nitro-fatty acids. Nitric Oxide 78, 170 175. Desikan, R., Griffiths, R., Hancock, J., Neill, S., 2002. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 99, 16314 16318. Diao, Q.-n, Song, Y.-j, Shi, D.-m, Qi, H.-y, 2016. Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum Mill.) seedling. J. Zhejiang Univ.—Sci. B 17, 916 930. Domingos, P., Prado, A.M., Wong, A., Gehring, C., Feijo, J.A., 2015. Nitric oxide: a multitasked signaling gas in plants. Mol. Plant 8, 506 520. Du, S., Zhang, R., Zhang, P., Liu, H., Yan, M., Chen, N., et al., 2016. Elevated CO2-induced production of nitric oxide (NO) by NO synthase differentially affects nitrate reductase activity in Arabidopsis plants under different nitrate supplies. J. Exp. Bot. 67, 893 904. Esim, N., Atici, O., Mutlu, S., 2014. Effects of exogenous nitric oxide in wheat seedlings under chilling stress. Toxicol. Ind. Health 30, 268 274. Espunya, M.C., De Michele, R., Go´mez-Cadenas, A., Martı´nez, M.C., 2012. S-Nitrosoglutathione is a component of wound- and salicylic acid-induced systemic responses in Arabidopsis thaliana. J. Exp. Bot. 63, 3219 3227. Fancy, N.N., Bahlmann, A.-K., Loake, G.J., 2016. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 40, 462 472. Fares, S., Vargas, R., Detto, M., Goldstein, A.H., Karlik, J., Paoletti, E., et al., 2013. Tropospheric ozone reduces carbon assimilation in trees: estimates from analysis of continuous flux measurements. Global Change Biol. 19, 2427 2443. Ferrarini, A., De Stefano, M., Baudouin, E., Pucciariello, C., Polverari, A., Puppo, A., et al., 2008. Expression of Medicago truncatula genes responsive to nitric oxide in pathogenic and symbiotic conditions. Mol. Plant Microbe Interact. 21, 781 790. Foresi, N., Correa-Aragunde, N., Parisi, G., Calo´, G., Salerno, G., Lamattina, L., 2011. Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22, 3816 3830. Fu, Y.-F., Zhang, Z.-W., Yuan, S., 2018. Putative connections between nitrate reductase S-nitrosylation and no synthesis under pathogen attacks and abiotic stresses. Front. Plant Sci. 9, 474. Gall, J.E., Boyd, R.S., Rajakaruna, N., 2015. Transfer of heavy metals through terrestrial food webs: a review. Environ. Monit. Assess. 187, 201. Gaupels, F., Furch, A.C., Zimmermann, M.R., Chen, F., Kaever, V., Buhtz, A., et al., 2016. Systemic induction of NO-, redox-, and cGMP signaling in the pumpkin extrafascicular phloem upon local leaf wounding. Front. Plant Sci. 7, 154.

Plant Life under Changing Environment

References

751

Gaupels, F., Durner, J., Kogel, K.-H., 2017. Production, amplification and systemic propagation of redox messengers in plants? The phloem can do it all!. New Phytol. 214, 554 560. Gould, K.S., Lamotte, O., Klinguer, A., Pugin, A., Wendehenne, D., 2003. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26, 1851 1862. Gow, A.J., Farkouh, C.R., Munson, D.A., Posencheg, M.A., Ischiropoulos, H., 2004. Biological significance of nitric oxide-mediated protein modifications. Am. J. Physiol.—Lung Cell. Mol. Physiol. 287, L262 L268. GroB, F., Durner, J., Gaupels, F., 2013. Nitric oxide, antioxidants and prooxidants in plant defence responses. Front. Plant Sci. 4, 419. Guo, F.-Q., Okamoto, M., Crawford, N.M., 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100 103. Gupta, K.J., Igamberdiev, A.U., 2011. The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion 11, 537 543. Gupta, K.J., Stoimenova, M., Kaiser, W.M., 2005. In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. J. Exp. Bot. 56, 2601 2609. Gupta, K.J., Fernie, A.R., Kaiser, W.M., van Dongen, J.T., 2011. On the origins of nitric oxide. Trends Plant Sci. 16, 160 168. Hao, F., Zhao, S., Dong, H., Zhang, H., Sun, L., Miao, C., 2010. Nia1 and Nia2 are involved in exogenous salicylic acid-induced nitric oxide generation and stomatal closure in Arabidopsis. J. Integr. Plant Biol. 52, 298 307. He, Y., Tang, R.-H., Hao, Y., Stevens, R.D., Cook, C.W., Ahn, S.M., et al., 2004. Nitric oxide represses the Arabidopsis floral transition. Science 305, 1968 1971. He, H., He, L., Gu, M., 2014. The diversity of nitric oxide function in plant responses to metal stress. Biometals 27, 219 228. Hess, D.T., Matsumoto, A., Kim, S.-O., Marshall, H.E., Stamler, J.S., 2005. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150 166. Houmani, H., Rodriguez-Ruiz, M., Palma, J.M., Corpas, F.J., 2018. Mechanical wounding promotes local and long distance response in the halophyte Cakile maritima through the involvement of the ROS and RNS metabolism. Nitric Oxide 74, 93 101. Huang, X., Stettmaier, K., Michel, C., Hutzler, P., Mueller, M.J., Durner, J., 2004. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218, 938 946. Hussain, A., Mun, B.-G., Imran, Q.M., Lee, S.-U., Adamu, T.A., Shahid, M., et al., 2016. Nitric oxide mediated transcriptome profiling reveals activation of multiple regulatory pathways in Arabidopsis thaliana. Front. Plant Sci. 7, 975. Imran, Q.M., Hussain, A., Lee, S.-U., Mun, B.-G., Falak, N., Loake, G.J., et al., 2018. Transcriptome profile of NOinduced Arabidopsis transcription factor genes suggests their putative regulatory role in multiple biological processes. Sci. Rep. 8, 771. Jaggard, K.W., Qi, A., Ober, E.S., 2010. Possible changes to arable crop yields by 2050. Philos. Trans. R. Soc. London, Ser. B 365, 2835 2851. Jeandroz, S., Wipf, D., Stuehr, D.J., Lamattina, L., Melkonian, M., Tian, Z., et al., 2016. Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Sci. Signal. 9, re2. Kangasjarvi, J., Jaspers, P., Kollist, H., 2005. Signalling and cell death in ozone-exposed plants. Plant Cell Environ. 28, 1021 1036. Kawabe, H., Ohtani, M., Kurata, T., Sakamoto, T., Demura, T., 2018. Protein S-nitrosylation regulates xylem vessel cell differentiation in Arabidopsis. Plant Cell Physiol. 59, 17 29. Khan, M.N., Siddiqui, M.H., Mohammad, F., Naeem, M., 2012. Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27, 210 218. Klepper, L., 1979. Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos. Environ. (1967) 13, 537 542. Kolbert, Z., Erdei, L., 2008. Involvement of nitrate reductase in auxin-induced NO synthesis. Plant Signaling Behav. 3, 972 973. Kolbert, Z., Ortega, L., Erdei, L., 2010. Involvement of nitrate reductase (NR) in osmotic stress-induced NO generation of Arabidopsis thaliana L. roots. J. Plant. Physiol. 167, 77 80. Kopyra, Mg, Gwozdz, E.A., 2003. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant. Physiol. Biochem. 41, 1011 1017.

Plant Life under Changing Environment

752

29. Nitric oxide under abiotic stress conditions

Kramer, U., Clemens, S., 2005. Molecular biology of metal homeostasis and detoxification. In: Tamas, M., Martinoia, E. (Eds.), Topics in Current Genetics. Springer Verlag, New York, pp. 216 271. Krasuska, U., Ciacka, K., Andryka-Dudek, P., Bogatek, R., Gniazdowska, A., 2015. Nitrosative door in seed dormancy alleviation and germination. In: Gupta, K., Igamberdiev, A. (Eds.), Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants. Springer, Switzerland, pp. 215 237. Krasuska, U., Ciacka, K., Gniazdowska, A., 2017. Nitric oxide-polyamines cross-talk during dormancy release and germination of apple embryos. Nitric Oxide 68, 38 50. Langerbartels, C., Wohlgemuth, H., Kschieschan, S., Grun, S., Sandermann, H., 2002. Oxidative burst and cell death in ozone-exposed plants. Plant. Physiol. Biochem. 40, 567 575. Lee, U., Wie, C., Fernandez, B.O., Feelisch, M., Vierling, E., 2008. Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20, 786 802. Leshem, Y.A.Y., Wills, R.B.H., Ku, V.V.-V., 1998. Evidence for the function of the free radical gas—nitric oxide (NO•)—as an endogenous maturation and senescence regulating factor in higher plants. Plant. Physiol. Biochem. 36, 825 833. Li, W., Liu, X., Ajmal Khan, M., Yamaguchi, S., 2005. The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. J. Plant. Res. 118, 207 214. Li, X., Pan, Y., Chang, B., Wang, Y., Tang, Z., 2016. NO promotes seed germination and seedling growth under high salt may depend on EIN3 protein in Arabidopsis. Front. Plant Sci. 6, 1203. Li, B., Gao, K., Ren, H., Tang, W., 2018a. Molecular mechanisms governing plant responses to high temperatures. J. Integr. Plant Biol. 60, 757 779. Li, C., Song, Y., Guo, L., Gu, X., Muminov, M.A., Wang, T., 2018b. Nitric oxide alleviates wheat yield reduction by protecting photosynthetic system from oxidation of ozone pollution. Environ. Pollut. 236, 296 303. Lin, C.C., Jih, P.J., Lin, H.H., Lin, J.S., Chang, L.L., Shen, Y.H., et al., 2011. Nitric oxide activates superoxide dismutase and ascorbate peroxidase to repress the cell death induced by wounding. Plant Mol. Biol. 77, 235 249. Lindermayr, C., 2017. Crosstalk between reactive oxygen species and nitric oxide in plants: key role of S-nitrosoglutathione reductase. Free Radical Biol. Med. 122, 110 115. pii: S0891-5849: 31231-31235. Lindermayr, C., Durner, J., 2015. Interplay of reactive oxygen species and nitric oxide: nitric oxide coordinates reactive oxygen species homeostasis. Plant Physiol. 167, 1209 1210. Liu, H.-T., Sun, D.-Y., Zhou, R.-G., 2005. Ca2 1 and AtCaM3 are involved in the expression of heat shock protein gene in Arabidopsis. Plant Cell Environ. 28, 1276 1284. Liu, Y., Jiang, H., Zhao, Z., An, L., 2010. Nitric oxide synthase like activity-dependent nitric oxide production protects against chilling-induced oxidative damage in Chorispora bungeana suspension cultured cells. Plant. Physiol. Biochem. 48, 936 944. Liu, X., Liu, B., Xue, S., Cai, Y., Qi, W., Jian, C., et al., 2016. Cucumber (Cucumis sativus L.) nitric oxide synthase associated gene1 (CsNOA1) Plays a role in chilling stress. Front. Plant Sci. 7, 1652. Lozano-Juste, J., Leon, J., 2010. Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. 152, 891 903. Manai, J., Gouia, H., Corpas, F.J., 2014. Redox and nitric oxide homeostasis are affected in tomato (Solanum lycopersicum) roots under salinity-induced oxidative stress. J. Plant. Physiol. 171, 1028 1035. Mata-Perez, C., Sanchez-Calvo, B., Begara-Morales, J.C., Carreras, A., Padilla, M.N., Melguizo, M., et al., 2016a. Nitro-linolenic acid is a nitric oxide donor. Nitric Oxide 57, 57 63. Mata-Perez, C., Sanchez-Calvo, B., de las Nieves Padilla-Serrano, M., Begara-Morales, J.C., Luque, F., Melguizo, M., et al., 2016b. Nitro-fatty acids in plant signaling: nitro-linolenic acid induces the molecular chaperone network in Arabidopsis. Plant Physiol. 170, 686 701. Montilla-Bascon, G., Rubiales, D., Hebelstrup, K.H., Mandon, J., Harren, F.J.M., Cristescu, S.M., et al., 2017. Reduced nitric oxide levels during drought stress promote drought tolerance in barley and is associated with elevated polyamine biosynthesis. Sci. Rep. 7, 13311. Moreau, M., Lee, G.I., Wang, Y., Crane, B.R., Klessig, D.F., 2008. AtNOS/A1 is a functional Arabidopsis thaliana cGTPase and not a nitric oxide synthase. J. Biol. Chem. 283, 32957 32967. Mur, L.A.J., Mandon, J., Persijn, S., Cristescu, S.M., Moshkov, I.E., Novikova, G.V., et al., 2013. Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5, pls052.

Plant Life under Changing Environment

References

753

Nahar, K., Hasanuzzaman, M., Suzuki, T., Fujita, M., 2017. Polyamines-induced aluminum tolerance in mung bean: a study on antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology 26, 58 73. Ortega-Galisteo, A.P., Rodriguez-Serrano, M., Pazmin˜o, D.M., Gupta, D.K., Sandalio, L.M., Romero-Puertas, M.C., 2012. S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J. Exp. Bot. 63, 2089 2103. Parani, M., Rudrabhatla, S., Myers, R., Weirich, H., Smith, B., Leaman, D.W., et al., 2004. Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant. Biotechnol. J. 2, 359 366. Parankusam, S., Adimulam, S.S., Bhatnagar-Mathur, P., Sharma, K.K., 2017. Nitric oxide (NO) in plant heat stress tolerance: current knowledge and perspectives. Front. Plant Sci. 8, 1582. Peto, A., Lehotai, N., Feigl, G., Tugyi, N., Ordog, A., Gemes, K., et al., 2013. Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis. Plant Cell Rep. 32, 1913 1923. Planchet, E., Jagadis Gupta, K., Sonoda, M., Kaiser, W.M., 2005. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J. 41, 732 743. Polverari, A., Molesini, B., Pezzotti, M., Buonaurio, R., Marte, M., Delledonne, M., 2003. Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol. Plant Microbe. Interact. 16, 1094 1105. Procha´zkova´, D., Sumaira, J., Wilhelmova´, N.A., Pavlı´kova´, D., Sza´kova´, J., 2014. Reactive nitrogen species and the role of NO in abiotic stress. In: Ahmad, P. (Ed.), Emerging Technologies and Management of Crops Stress Tolerance. Elsevier. Puyaubert, J., Fares, A., Reze, N., Peltier, J.B., Baudouin, E., 2014. Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: effect of cold stress on cysteine nitrosylation level. Plant Sci. 215 216, 150 156. Radi, R., 2004. Nitric oxide, oxidants, and protein tyrosine nitration. Proc. Natl. Acad. Sci. U.S.A. 101, 4003 4008. Rodriguez-Serrano, M., Romero-Puertas, M.C., Pazmino, D.M., Testillano, P.S., Risueno, M.C., Del Rio, L.A., et al., 2009. Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol. 150, 229 243. Sahay, S., Gupta, M., 2017. An update on nitric oxide and its benign role in plant responses under metal stress. Nitric Oxide 67, 39 52. Santisree, P., Bhatnagar-Mathur, P., Sharma, K.K., 2015. NO to drought-multifunctional role of nitric oxide in plant drought: do we have all the answers? Plant Sci. 239, 44 55. Santolini, J., Andre´, F., Jeandroz, S., Wendehenne, D., 2017. Nitric oxide synthase in plants: Where do we stand? Nitric Oxide 63, 30 38. Savatin, D.V., Gramegna, G., Modesti, V., Cervone, F., 2014. Wounding in the plant tissue: the defense of a dangerous passage. Front. Plant Sci. 5, 470. Sehrawat, A., Abat, J.K., Deswal, R., 2013. RuBisCO depletion improved proteome coverage of cold responsive Snitrosylated targets in Brassica juncea. Front. Plant Sci. 4, 342. Selvarajan, D., Mohan, C., Dhandapani, V., Nerkar, G., Jayanarayanan, A.N., Vadakkancherry Mohanan, M., et al., 2018. Differential gene expression profiling through transcriptome approach of Saccharum spontaneum L. under low temperature stress reveals genes potentially involved in cold acclimation. 3 Biotech. 8, 195. Shi, H., Ye, T., Zhu, J.-K., Chan, Z., 2014. Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J. Exp. Bot. 65, 4119 4131. Signorelli, S., Corpas, F.J., Borsani, O., Barroso, J.B., Monza, J., 2015. Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus. Plant Sci. 201-202, 137 146. Signorelli, S., Corpas, F.J., Rodriguez-Ruiz, M., Valderrama, R., Barroso, J.B., Borsani, O., et al., 2018. Drought stress triggers the accumulation of NO and SNOs in cortical cells of Lotus japonicus L. roots and the nitration of proteins with relevant metabolic function. Environ. Exp. Bot. Available from: https://doi.org/10.1016/ j.envexpbot.2018.1008.1007. Singh, P.K., Indoliya, Y., Chauhan, A.S., Singh, S.P., Singh, A.P., Dwivedi, S., et al., 2017. Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress. Sci. Rep. 7, 3592. Sparacino-Watkins, C.E., Tejero, J., Sun, B., Gauthier, M.C., Thomas, J., Ragireddy, V., et al., 2014. Nitrite reductase and nitric-oxide synthase activity of the mitochondrial molybdopterin enzymes mARC1 and mARC2. J. Biol. Chem. 289, 1345 1358.

Plant Life under Changing Environment

754

29. Nitric oxide under abiotic stress conditions

Stohr, C., Strube, F., Marx, G., Ullrich, W.R., Rockel, P., 2001. A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212, 835 841. Stoimenova, M., Igamberdiev, A.U., Gupta, K.J., Hill, R.D., 2007. Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226, 465 474. Tanou, G., Job, C., Rajjou, L., Arc, E., Belghazi, M., Diamantidis, G., et al., 2009. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J. 60, 795 804. Tanou, G., Filippou, P., Belghazi, M., Job, D., Diamantidis, G., Fotopoulos, V., et al., 2012. Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J. 72, 585 599. Tun, N.N., Santa-Catarina, C., Begum, T., Silveira, V., Handro, W., Floh, E.I., et al., 2006. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana. Plant Cell Physiol. 47, 346 354. Vainonen, J.P., Kangasjarvi, J., 2015. Plant signalling in acute ozone exposure. Plant Cell Environ. 38, 240 252. Valderrama, R., Corpas, F.J., Carreras, A., Ferna´ndez-Ocan˜a, A., Chaki, M., Luque, F., et al., 2007. Nitrosative stress in plants. FEBS Lett. 581, 453 461. Vanzo, E., Ghirardo, A., Merl-Pham, J., Lindermayr, C., Heller, W., Hauck, S.M., et al., 2014. S-Nitroso-proteome in poplar leaves in response to acute ozone stress. PLoS One 9, e106886. Wang, L., Guo, Y., Jia, L., Chu, H., Zhou, S., Chen, K., et al., 2014. Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. Plant Physiol. 164, 2184 2196. Wang, P., Du, Y., Hou, Y.-J., Zhao, Y., Hsu, C.-C., Yuan, F., et al., 2015a. Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc. Natl. Acad. Sci. U.S.A. 112, 613 618. Wang, P., Zhu, J.-K., Lang, Z., 2015b. Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by S-nitrosylation of SnRK2 proteins. Plant Signaling Behav. 10, e1031939. Wimalasekera, R., Tebartz, F., Scherer, G., 2011. Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci. 181, 593 603. Xie, Y., Mao, Y., Lai, D., Zhang, W., Zheng, T., Shen, W., 2013. Roles of NIA/NR/NOA1-dependent nitric oxide production and HY1 expression in the modulation of Arabidopsis salt tolerance. J. Exp. Bot. 64, 3045 3060. Xuan, Y., Zhou, S., Wang, L., Cheng, Y., Zhao, L., 2010. Nitric oxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiol. 153, 1895 1906. Yamasaki, H., Sakihama, Y., 2000. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett. 468, 89 92. Yang, H., Mu, J., Chen, L., Feng, J., Hu, J., Li, L., et al., 2015. S-Nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol. 167, 1604 1615. Yu, M., Lamattina, L., Spoel, S.H., Loake, G.J., 2014. Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol. 202, 1142 1156. Zhang, Y., Wang, L., Liu, Y., Zhang, Q., Wei, Q., Zhang, W., 2006. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na 1 /H 1 antiport in the tonoplast. Planta 224, 545 555. Zhang, W., Zhou, R.G., Gao, Y.J., Zheng, S.Z., Xu, P., Zhang, S.Q., et al., 2009. Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis. Plant Physiol. 149, 1773 1784. Zhao, L., Zhang, F., Guo, J., Yang, Y., Li, B., Zhang, L., 2004. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol. 134, 849 857. Zhao, M.-G., Chen, L., Zhang, L.-L., Zhang, W.-H., 2009. Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol. 151, 755 767.

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30 Role of metabolites in abiotic stress tolerance ´ gnes Szepesi A Department of Plant Biology, Institute of Biology, University of Szeged, Szeged, Hungary

30.1 Abiotic stress tolerance In order to combat against climate change and make efforts to maintain sustainable agriculture and provide enough safe food and feed, researchers focus on deciphering the exact tolerance processes against plant abiotic stress (Amaˆncio et al., 2017). There are a lot of technologies which are applied to improve the stress tolerance of our crop plants, but the understanding of the background of the abiotic stress tolerance needs great efforts. In order to use the plant-derived metabolites as a biostimulant or bioeffector compounds, we have to gain better insight into their complex regulation and metabolism. Comprehensive “omics” techniques focusing on metabolites are useful analysis in order to increase our knowledge of abiotic stress tolerance. The function of all specialized metabolites is also need to be investigated. It is important to note that these data come from the precise analysis and may require the investigation of field-grown plants. This chapter will focus on some of the most important metabolites which can influence the plant abiotic stress tolerance processes and some of special metabolites the role of which suggest that they could be the next generation of metabolites involved in improving climate resilient crops.

30.2 Primary metabolites and osmoprotectants Most of the research studies, involved in improving the abiotic stress tolerance, have been focused on the carbohydrates and amino acids, as primary metabolites in plant stress tolerance. During photosynthesis, carbohydrates are produced and used as energy storage. Amino acids, as N-containing molecules are also precursors of plant metabolites related to plant defense.

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In an experiment conducted by Moles et al. (2018), the drought induced changes of leafto-root relationships were investigated in two different tomato genotypes. Some agronomic traits of Triticum aestivum, Triticale, and Tritipyrum species were investigated by Shanazari et al. (2018) during drought stress. Annunziata et al. (2017) studied the adaptation responses of durum wheat roots to salinity. They described that durum wheat roots could remodel the N-containing metabolites and cellular sucrose content. It is well established that the temperature stress can affect the physiology of plants. Li et al. (2018a,b) investigated two zoyziagrass genotypes native to high and low latitudes in order to compare the physiological and metabolic responses to low temperature. Heat stress induced adaptation of wheat grains by metabolomics manner contributes to a stable filling rate (Wang et al., 2018a,b). In the study by Ferchichi et al. (2018), two different barley species were compared in their responses to extended salinity stress, and it was found that they display different accumulation time of metabolites.

30.2.1 Carbohydrates Fine tuning of carbohydrate homeostasis is a critical process, and it is important to study in plant-stress tolerance (Pommerrenig et al., 2018). Van den Ende (2014) suggested that the central position of sugars in apical dominance during plant growth, development, and stress responses strongly depends on sugars. Zhang et al. (2018a,b) investigated the desiccation tolerance of Oropetium thomaeum grass during different environmental stresses, and they found that sugar metabolism under dehydration induced similar effects such as low temperature and salt stress. They also found that sugar metabolism in O. thomaeum showed some stress-specific responses. Treatment with abscisic acid (ABA) induced substantial synthesis of stachyose after the dehydration, so it is suggested that stachyose synthesis is connected to ABA signal pathway in O. thomaeum (Zhang et al., 2018a,b). 30.2.1.1 Trehalose Trehalose is one of the most important compatible metabolites from algae to higher plants and plays a signal role in many interactions between plant and microorganisms or herbivorous insects (Lunn et al., 2014). As the functions of trehalose have some overlapping features with sucrose in vascular plants, Figueroa and Lunn (2016) reported the recent findings of two these important sugars, the trehalose-6-phosphate (Tre6P), and sucrose in their review. Tre6P, which is one of the intermediate metabolites of trehalose biosynthesis, can affect photosynthesis and the partitioning of assimilates in reproductive tissue (Oszvald et al., 2018). Tre6P signal pathway is important to move carbon from leaf to kernel in field studies (Smeekens, 2015). Xu et al. (2017a,b) investigated the gene family of Tre6P synthase (TPS) in Solanum tuberosum (potato) by genome-wide association study, and they revealed the evolution and differential expression during the development and stress in potato. The characterization of this gene family was conducted by Xie et al. (2015) and expression analysis during freezing stress in winter wheat demonstrating that this enzyme has an important role in freezing stress. Lunn et al. (2014) summarized the balance between sucrose and starch is affected by Tre6P, which also influences the mechanism of starch degradation. The importance of Tre6P is highlighted by the evidence that mutant plants defected in its

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metabolism have strongly pleiotropic phenotype and show abnormal embryogenesis and leaf growth, and some defections in reproductive system (Lunn et al., 2014). Trehalose also influences the cold and salinity responses, for example, stomatal opening and water-use efficiency. Delorge et al. (2014) suggested that regulating the trehalose biosynthesis and the rate of hydrolysis can be a useful tool for the production of better tolerant plants against abiotic stress. Analysis of trehalose contents and the biosynthesis gene family between the species analysis by Han et al. (2016) revealed that trehalose has a crucial role in tolerant cassava plants during osmotic stress. This compound was capable to improve the growth of plants in N-deficient conditions by upregulating the nitrogen metabolism (Lin et al., 2017). Trehalose metabolism has different role in source and sink tissues of salt stressed plants, indicated evidence in maize by Henry et al. (2015). Trehalose-6-phosphate phosphatase in Arabidopsis thaliana (AtTPPD), which is a redox-sensitive, chloroplast localized Tre6P phosphatase, has a role in regulation of salt-stress tolerance (Krasensky et al., 2014). Trehalose was efficient as a pretreatment to induce salt tolerance in rice seedlings (Mostofa et al., 2015). Chilling stress caused a delayed germination time in Arabidopsis seeds when a gene called abiotic stress inducible GhTPS11 was over expressed (Wang et al., 2016). Also, trehalose was used as an exogenous treatment compound in order to trigger resistance against downy mildew disease of pearl millet by activating the defense-related enzymes (Govind et al., 2016). 30.2.1.2 Starch Starch is considered as the major carbohydrate storage in plants with many important role (Goren et al., 2018). McKinley et al. (2018) investigated the developmental dynamics of stem starch accumulation in Sorghum bicolor. Starch is one of the determinants of fitness in abiotic stress exposed plants (Thalmann and Santelia, 2017). The biosynthesis of starch and the modification of granule assembly in plants are in interest of wide range of industry contributed to evolve products connected to human and animal nutrition, pharmaceuticals (Huang et al., 2018). New evidence suggests that the regulation of starch metabolism is regulated by an Arabidopsis circadian oscillator using sugar signaling (Seki et al., 2017). 30.2.1.3 Fructans Fructans are fructose-based multifunctional carbohydrates which have a role in plant abiotic stress tolerance. Our knowledge about fructan production and the precise mechanisms involved in fructan induced stress tolerance is limited as suggested by the work of Versluys et al. (2018). Fructans can be a mean of salt-stress tolerance during salt exposure (Kirtel et al., 2018). Livingston et al. (2009) summarized the proposed functions of these carbohydrates in plants not just in salt stress but in other abiotic stress tolerance mechanisms as well. Fructans can act as reserve carbohydrates in crop plants suggested by Housley et al. (2017). Veenstra et al. (2017) suggested that wheat fructans can be good candidates for potential breeding targets for producers to develop nutritionally improved and climate-resilient varieties. 30.2.1.4 Raffinose family oligosaccharides Raffinose and stachyose, the members of the raffinose family of oligosaccharides (RFOs), were reported that they can act as energy metabolites in plant seeds and are

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compounds released during the plant-germination process (Sengupta et al., 2015). Galactinol synthase can produce galactinol (Nishizawa et al., 2008), which is also reported that has a crucial role in plant development as well as in tolerance against drought and temperature stresses (Taji et al., 2002; Iba´n˜ez et al., 2013). Galactose can act as a storage metabolite of RFOs in seeds, and they suggested that these oligosaccharides results in rapid germination of Arabidopsis in the dark (Gangl and Tenhaken, 2016). These data suggest the different regulation of these oligosaccharides dependent on light and dark conditions. Nowadays, there is an increasing data about the potential role of plant RFOs biosynthesis and galactinol production in plants (Sengupta et al., 2015). Egert et al. (2013) found evidence that a single raffinose synthase (RS5, At5g40390) resulted in abiotic stress induced accumulation of raffinose in Arabidopsis leaves. Importance of RFOs in stress tolerance processes was proved by George et al. (2018) in Macrotyloma uniflorum during abiotic stresses, for example, drought and salt stress. These responses lead to common and specific transcriptomic responses. Sun et al. (2018) deciphered that the GARP/MYB-related AQUILO grape transcription factor improves cold tolerance and induced accumulation of RFOs. Raffinose synthase genes in sugar beet were isolated, functionally characterized, and reported their stress responses by Kito et al. (2018).

30.2.2 Amino acids 30.2.2.1 Proline The most extensively studied amino acid is proline (Pro) in plant abiotic stress tolerance (Fichman et al., 2015). Per et al. (2017) summarized the studies that approach the modulation of Pro metabolism in plants under salt- and drought-stress tolerance and at the same time also related to phytohormones, mineral nutrients, or transgenic approach. Recently, ˝ osi ˝ (2018) described the plant Pro biosynthesis and its metabolism under Szepesi and Szoll stress conditions. Singh et al. (2017) described the role of Pro as osmolytes in plants as a sensors of abiotic stress. Exogenous Pro treatment induced salt tolerance in maize induced low oxidative damage and favorable ionic homeostasis (de Freitas et al., 2018). Zali et al. (2018) demonstrated that grain yield and essential oil composition were dependent from genotypes to Pro treatment in different conditions in Foeniculum vulgare. An interesting experiment was conducted by Semida et al. (2018) who found that cadmium tolerance was elevated by sequenced ascorbate-Pro-glutathione seed treatment in cucumber transplants. Further investigation of Pro as a seed presoaking treatment or combined with other antioxidant compounds may help us to alleviate stress injury of crop plants limiting the yield loss in agriculture. 30.2.2.2 γ-Amino-N-butyric acid One of the most important nonprotein amino acid is the γ-amino-N-butyric acid (GABA). Carillo (2018) summarized the GABA shunt in durum wheat and investigated the evidences of mechanisms under salinity stress and high light. Farooq et al. (2017) studied bread wheat plants during drought stress, and they found that exogenous application of Pro and GABA was effective to elevate resistance against drought. In Brassica juncea L.,

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GABA modulated the antioxidant defense and glyoxalase systems alleviating the chromium stress (Mahmud et al., 2017). The experimental evidence suggests a role of the protective effect of exogenous GABA treatment against drought stress (Li et al., 2018a,b; Cheng et al., 2018; Rezaei-Chiyaneh et al., 2018), salt stress (Ji et al., 2018), anoxia, and low light stress (Liao et al., 2017; Li et al., 2017).

30.2.3 Sugar alcohols (polyols): myo-inositol, D-pinitol 30.2.3.1 Cyclitols: myo-inositol and pinitol Myo-inositol is one of the D-pinitol’s precursors. Recently, the role of D-pinitol in reproductive stage was examined in a study by Dumschott et al. (2018). They have suggested that comparing three chickpea genotypes in field conditions, D-pinitol was the most abundant sugar alcohol. Guo et al. (2018) made an observation with sweet sorghum, and they found that photosystem II of plants was protected by energy dissipation and effective antioxidant enzyme system during drought stress. 30.2.3.2 Alditols: mannitol and sorbitol Alditols are open chain sugar alcohols have been given more attention nowadays (Dumschott et al., 2017). Sorbitol and mannitol, some of the special alditols, can be affected by environmental conditions and sink source transitions (Loescher and Everard, 2000). For example, Tari et al. (2010) proved that aldose reductase activity showed increased activity and accumulated sorbitol after exogenously applied salicylic acid treatment in salt stress exposed tomato plants. JrVHAG1, a gene coding a vacuolar H1-ATPase G subunit from Juglans regia, is involved in the tolerance for mannitol-induced osmotic stress (Xu et al., 2017a,b). Exogenously applied mannitol could regulate plant development and salinity stress induced oxidative stress responses in maize (Kaya et al., 2013).

30.2.4 Glycine betaine, an osmotic adjustment substance Glycine betaine (GB) is a quaternary ammonium compound, which can influence the maintenance of cell osmotic pressure, protection of proteins, and regulation of stress responses (Mansour, 1998). GB was effective to counteract the effect of water logging on tomato fruits as the growth, oxidative defense system, and nutrient composition were investigated (Rasheed et al., 2018). Nowadays, intensive research has started to decipher the precise mechanism and role of betain aldehyde dehydrogenase in plants. Liu et al. (2018a,b) isolated and characterized salt stress related changes of a betaine aldehyde dehydrogenase in Lycium ruthenicum Murr. species. Qin et al. (2017) also examined those transgenic soybeans expressing that the betaine-aldehyde dehydrogenase from Atriplex canescens showed better tolerance against drought. Mansour and Ali (2017) assessed the current state of knowledge about GB in saline conditions. Wei et al. (2017) showed that engineering genetically the biosynthesis of GB was efficient by alleviated salt-induced potassium efflux and therefore contributed to better salt tolerance of tomato plants. Castiglioni et al. (2018) identified GB1, a gene which could increase GB content in maize and soybean by its constitutive over expression. Ethanolamine was efficient to modify GB

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content and prometabolism in Nicotiana rustica during salt stress (Rajaeian et al., 2017). Zouari et al. (2018) found that exogenous Pro induced better tolerance against lead stress than GB in the case of olive trees. Tian et al. (2017) reported that thylakoid membranes function better by overaccumulating GB in salt-stressed wheat plants. Exogenously applied Pro and GB affected the nodule activity of soybean under salt stress (Sabagh et al., 2017). Commercial tomato genotypes were investigated that how they are influenced by Pro and GB metabolism on tolerance to salt stress (De la Torre-Gonza´lez et al., 2018). Effects of GB and the polyamine (PA) spermidine were compared on osmotic adjustment and antioxidant-defense processes, which could improve the drought tolerance of creeping bent grass by Liu et al. (2017). Foliar-applied GB upregulated the antioxidants that contributed to the better tolerance to salt-stressed onions (Rady et al., 2018). Phillips et al. (2018) investigated maize plants that inhibition of nitric oxide synthase (NOS)-like activity altered gene expressions involved in H2O2 scavenging and GB biosynthesis. There are some data that GB treatment could act as a postharvest treatment as well. Yao et al. (2018) showed that chilling injury was alleviated by GB treatment in zucchini fruit (Cucurbita pepo L.) affecting antioxidant enzyme activities. Cheng et al. (2018) made experiments with GB, and they found that seed treatment with GB enhances tolerance of cotton to chilling stress. Wang et al. (2019) demonstrated that peach fruits injured by chilling stress showed enhanced phenolic and sugar metabolisms by GB treatment. GB treatment also affected membrane fatty acid metabolism in chilling injured zucchini fruit (C. pepo L.) (Yao et al., 2018). Kaya et al. (2018) used combined treatment of nitric oxide and thiamin, and they have found that this type of treatment can positively regulate some physiological parameters and antioxidants in maize cultivars with different salinity tolerance. Xu et al. (2018) provided data in watermelon suspension cells that GB biosynthesis depends on jasmonate signaling during osmotic stress. Hisyam et al. (2017) reported that GB could have effect on antioxidants and gene function in Oryza sativa during water stress. Experimental evidence by Xalxo et al. (2017) suggests that GB and aspirin could modulate the nickel toxicity in Pennisetum typhoideum. GB could improve antioxidant enzyme activities, as well as Pro and genomic template stability by inducing reduced oxidative injury during fluoride stress in Cajanus cajan plants (Yadu et al., 2017). Enhanced tolerance of Arabidopsis was gained by betaine aldehyde dehydrogenase gene from Ammopiptanthus nanus during salt and drought stress (Yu et al., 2017). Nutritional quality of hawthorn fruit was maintained during storage in low temperatures by GB treatment (Razavi et al., 2018).

30.2.5 Polyamines Numerous scientific evidences highlight the significance of PAs as hub molecules in abiotic stress tolerance. These polycations have multifunctional role from development to defense against many stress factors. The ameliorating effects of PA supplement in Stevia rebaudiana Bertoni were investigated by Moradi Peynevandi et al. (2018) under cold stress. Benavides et al. (2018) reported that PAs efficiently alleviate Cd and Cu stress-induced alterations in membranes of wheat and sunflower plants. Pa´l et al. (2018) investigated the interaction of PAs, ABA, and Pro under osmotic stress in the leaves of wheat plants. Espasandin et al. (2018) studied that overexpression of ADC gene (arginine decarboxylase)

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increased salt stress tolerance of Lotus tenuis plants. PA treatment effectively alleviated oxidative stress induced by gamma irradiation in Vigna radiata (Sengupta and Raychaudhuri, 2017). Moreover, PAs could efficiently alleviate oxidative stress-induced damage in the symbiosis Medicago truncatula Sinorhizobium meliloti which can contribute to increased salt tolerance (Lo´pez-Go´mez et al., 2017). PAs could contribute to induced phytochelatin synthesis during cadmium stress in rice (Pa´l et al., 2017). The PA metabolism of two agriculturally important crop, wheat and maize plant, was compared by Szalai et al. (2017). The effect of PAs can depend of plant salt sensitivity as described by Zapata et al. (2017). Zarza et al. (2017) studied mutant Arabidopsis thaliana seedlings in which the PA oxidase 5 gene is missing, and they suggested that these plants can tolerate salt stress by metabolic and transcriptional reprogramming. The connection between the PA biosynthetic pathways and salt stress tolerance in one of the most important monocot model plant, Brachypodium distachyon have been characterized by Takahashi et al. (2018). Freitas et al. (2018) investigated that ethylene could trigger salt tolerance in maize genotypes, and it was induced by modulated PA catabolism enzymes associated with H2O2 production.

30.2.6 New players in abiotic stress tolerance: melatonin and serotonin 30.2.6.1 Melatonin Melatonin, a derivative of tryptophan, was discovered in plants about 20 years ago, and nowadays there is an increasing evidence about the fact that endogenous indoleamines, melatonin and serotonin, are important in signal pathways of growth and development as well as in stress responses in plants (Wang et al., 2017). Erland et al. (2018) examined systematically the metabolic background of melatonin and serotonin in plant morphogenesis. Arnao and Herna´ndez-Ruiz (2018) described the role of melatonin and its relationship to plant hormones in plants. Table 30.1 summarizes that the plants that are involved to date in the experiments to gain better knowledge about the role of melatonin in plants. Herna´ndez-Ruiz and Arnao (2018) examined the possible relationship of melatonin and salicylic acid in biotic and abiotic stress conditions in plants. An interesting result came from the work of Lee et al. (2018) suggesting that flavonoids could inhibit not just sheep but also rice plant serotonin N-acetyltransferases resulting in reduced melatonin levels. Protective role of melatonin in the tolerance to stress combination in tomato plants was described by Martinez et al. (2018). 30.2.6.2 Serotonin Melatonin and serotonin have some overlapping regulatory roles in plant abiotic stress tolerance (Kaur et al., 2015). Erland et al. (2016) reported that serotonin is an ancient and important regulator molecule of plant developmental processes. Wan et al. (2018) provided insight into the effect of serotonin on Arabidopsis root growth and development. By analyzing metabolites of rice plants by Gupta and De (2017) during salt stress, an elevated serotonin and gentisic acid levels were detected in leaves of tolerant rice varieties. Molecular crosstalk mechanisms of these two important molecules, serotonin and

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TABLE 30.1 Experiments with melatonin in plants. Plant species

Developmental stage

Stress factor

References

Cucumber

Seed germination

High salinity

Zhang et al. (2017)

Tall fescue

Heat stress

Alam et al. (2018)

Solanum lycopersicum

High temperature

Ahammed et al. (2019)

Prunella vulgaris

Callogenesis

Malus hupehensis Rice

Fazal et al. (2018) Alkaline stress

Skotomorphogenesis

Gong et al. (2017) Hwang and Back (2018)

Tomato

Acid rain stress

Debnath et al. (2018)

Apple

Oxidative stress

Wei et al. (2018)

Kiwifruit

Senescence

Liang et al. (2018a,b)

Apple

Nutrient uptake

Arabidopsis thaliana

Leaf development

Wang et al. (2017)

Arabidopsis thaliana

Lateral root formation

Chen et al. (2018)

Morphogenesis

Erland and Saxena (2018)

Drought stress

Liang et al. (2018a,b)

melatonin, in plants were recently summarized by Mukherjee (2018). The investigation of regulatory roles of serotonin is an emerging area of research and requires great effort to decipher the exact role and mechanism of this compound in plant abiotic stress tolerance.

30.3 Role of secondary metabolites: antioxidants and defense compounds Abiotic stress signals have great influence on secondary metabolites in plants (Ramakrishna and Ravinshankar, 2011). Singer et al. (2016) summarized that the accumulation of storage lipids and their composition was strongly affected by abiotic factors. Triacylglycerols have some newly discovered functions in the plant developmental processes and stress conditions (Yang and Benning, 2018). A. thaliana plant lines with high oil content in their leaves responded differently to abiotic stress as suggested by Yurchenko et al. (2018). By applying transcriptomic and metabolite profiling, Savoi et al. (2016) revealed that white grapes (Vitis vinifera L.) showed altered phenylpropanoid and terpenoid pathways in response to prolonged drought stress. Xue et al. (2017) described how the molecular structure of cuticular wax was changed by evolution during drought tolerance. Ahmad et al. (2018) have found that salt stress in B. juncea can mitigate by zinc or calcium application inducing efficient antioxidant defense and glyoxalase systems. In mint (Tetradenia riparia), Bibbiani et al. (2018) investigated the Zn stress induced volatile organic compound emission, and they found that Zn did not change volatilome profile, but some compounds emitted higher rate, for example, methanol, acetylene, or propanal. Singh et al. (2018) investigated chickpea (Cicer arietinum L.) genotypes in order to get information

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about the osmotic, ionic stress mechanisms and some salt-responsive transcript components which can induce salinity tolerance. Selmar and Kleinwa¨chter (2013) summarized that stress factors could enhance the synthesis of secondary plant products. One of the most important processes in grass leaves is the bundle sheath suberization (Mertz and Brutnell, 2014). Enormous evidence suggests that ROS (reactive oxygen species) plays a crucial role in abiotic stress responses or stress combinations and tolerance mechanisms (Choudhury et al., 2017). Recently, it is inevitable to enhance nutrition values of our food crops and help fighting against abiotic stress, for example, with some modifications. Macknight et al. (2017) suggested that increasing ascorbate levels in crops could be a very successful mean of this process. Many excellent reviews reported the inevitable important tolerance mechanism of ascorbate glutathione cycle in plants exposed to abiotic stress (Akram et al., 2017; Bartoli et al., 2017; Zechmann, 2018). Pandey et al. (2017) summarized the multiple roles of ascorbate peroxidase in abiotic stress tolerance in plants. Liu et al. (2018a,b) reported that ascorbate peroxidase 6 gene from sugarcane, ScAPX6, regulates efficiently the abiotic stress responses in sugarcane. Growing evidence indicates that antioxidant mechanisms are sensitive to the light conditions. Zeng et al. (2018) showed that Arabidopsis seedlings deficient in ascorbate were more susceptible to high light-induced stress. Tari et al. (2015) described that salicylic acid effects showed time and organ-dependent antioxidant responses during alleviation of salt stress. Batth et al. (2017) studied the transcript profile of ascorbate oxidase genes and revealed the significance of abiotic stress and the dependence of the developmental stage of plants. In tobacco plants, enhanced abiotic stress tolerance has developed an after overexpression of Populus tomentosa cytosolic ascorbate peroxidase (Cao et al., 2017). Balfago´n et al. (2018) examined the combined stress of drought and high temperatures in citrus plants, and they found that tolerance could be induced by ascorbate peroxidase and heat-shock proteins. The importance of glucosinolates in Brassica species exposed to abiotic stress was reviewed by del Carmen Martı´nez-Ballesta et al. (2013). There are some examples which can explain why glucosinolates can be a good candidate for further investigation for improving and enhancing the abiotic stress tolerance of crop plants in the future. Palliyaguru et al. (2018) suggested that isothiocyanates can translate the power of plants to people. Urbancsok et al. (2017) provided evidence that isothiocyanates, which are derived from glucosinolates, could inhibit Arabidopsis growth depending from their side-chain structure. Cocetta et al. (2018) examined glucosinolates metabolism in wild rocket during heat stress and high salinity. Aghajanzadeh et al. (2018) investigated the different impacts of chloride and sulfate salinity on glucosinolate metabolism in Brassica rapa. George et al. (2017) also has found that in the case of Chrysopogon zizanioides, drought and salt stress affected essential oil composition and benzylisoquinoline alkaloids metabolism.

30.4 Conclusions and future prospects Engineering abiotic stress response in plants for biomass production is a very promising research area nowadays (Joshi et al., 2018). The compatible solute engineering of crop plants which are involved in improved tolerance toward abiotic stresses was summarized

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by Dutta et al. (2018). Derakhshani et al. (2017) reviewed multifunctional biomolecules with roles in abiotic stress tolerance and suggested their nutraceutical potential. Chemical priming is one of the most promising treatments which can affect and induce plant abiotic stress tolerance (Savvides et al., 2016). Chemical priming can significantly increase the yield components of drought stressed wheat plants (Sher et al., 2017). Hossain et al. (2017) described the key regulators and their possible mechanisms which are involved in heat or cold priming-induced cross-tolerance in plants exposed to abiotic stresses. Proteomic analyses in commercial crop plants are crucial to increase our knowledge of abiotic stress tolerance (Tan et al., 2017). The major factors which can determine alterations in cellular proteome during plant abiotic stress were investigated by Kosova´ et al. (2018). The role of secondary metabolites in plants, their transport, and self-tolerance mechanisms were described by Nobukazu (2016). Borges et al. (2017) summarized that in medicinal plants, the secondary metabolites synthesis is affected by the environmental factors. Moradi et al. (2017) made a metabolomic analysis in order to reveal the biochemical mechanisms underlying drought stress tolerance in thyme. AromaDb, a new database of medicinal and aromatic plant’s aroma molecules with chemical structure and therapeutic potentials, was introduced by Kumar et al. (2018). This database can direct the researchers to extensive investigation of the proper mechanisms of some significant compounds involved in aromatic plants. Growing evidence also indicates that metabolites can be applied as biostimulants and bioeffectors in order to alleviate the abiotic stress in crop plants (Van Oosten et al., 2017). Gerszberg and Hnatuszko-Konka (2017) reviewed those target sequences that are most often engineered in tomato that is one of the most important crop in horticulture. Sugar beet extract was used as a natural biostimulant in water-stressed wheat by Noman et al. (2018); this type of application could be a mean of sustainable development in agriculture in the future. Temporal accumulation pattern of metabolites still needs to be investigated in extensive manner to get deep insight into the stress responses between species with different sensitivity. A similar observation was made by Ferchichi et al. (2018) when they suggested that Hordeum vulgare and Hordeum maritimum respond to extended salinity stress displaying different temporal accumulation pattern of metabolites. Investigations of metabonomic phenotypes will elucidate some interspecies developmental differences, for example, in the case of L. ruthenicum and Lycium barbarum (Wang et al., 2018a,b). Tani et al. (2018) compared the seedling growth and transcriptional responses to salt shock and stress treatment of some Medicago species (M. sativa and M. arborea) and their hybrids. It is also important to decipher the exact role of metabolites in the plant cell wall structure remodeling in abiotic stress induced plants (Novakovi´c et al., 2018). There is still need to be investigated that how metabolites affect the metabolism of some cell wall related compounds, such as suberin under stress conditions (Graca, 2015). Excellent review from Byrt et al. (2018) described how the root cell wall of crop plants can respond to saline soils. Different transportome analysis will help us to gain better knowledge about how metabolites can interact and influence other compounds during stress conditions. de Brito Francisco and Martinoia (2018) summarized the vacuolar transportome of some specialized metabolites. Metabolomic analysis can help us to decipher new compounds with role in induction of abiotic stress tolerance mechanisms in plants. Mafu et al. (2018) reported the

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765 FIGURE 30.1 The pos-

Melatonin Heat stress radiation Drought stress Waterlogging Temperature stress Environmental pollutants

Root growth and development Salinity stress Heavy metal stress Insect resistance etc.

Serotonin Wounding Seed germination Somatic embryogenesis pathogens

sible overlapping effects of indoleamines (melatonin and serotonin) in plants. This figure describes some abiotic stress responses of these molecules, in which they can act simultaneously, such as the role in root growth and development, salinity stress, and insect resistance.

dolabradiene-derived defenses and the stress-induced accumulation of dolabradiene in maize. However, not just the accumulation but also the degradation of metabolites has a great impact on plant abiotic stress tolerance (Hildebrandt, 2018). Extensive investigation is needed to provide information about how secretory structures are involved in abiotic stress tolerance and how they could be modulated in order to produce more climate-resilient plants. Tissier (2018) suggested that plant secretory structures are more than just a reaction bags. Further evidences are needed to understand their role in this complex physiological background related to stress tolerance. The extra-pathway interactome of the tricarboxylic acid (TCA) cycle was revealed by Zhang et al. (2018a,b) with expected and unexpected metabolic interactions suggesting that this is just a beginning of better knowledge of exact role of TCA cycle related metabolites in stress management. Plants have to combat against the combination of stress factors, so the investigation of plant adaptations to combined stress factors is increasing interest among researchers. Strong efforts are being made to investigate the combinations of abiotic biotic stress responses (Suzuki et al., 2014). Zandalinas et al. (2018) reported a summary of plantadaptation mechanisms to combined drought and high temperature treatments (Fig. 30.1).

Acknowledgments This book chapter was financially supported by the European Union and the State of Hungary, cofinanced by the ´ MOP 4.2.4. A/2-11-1-2012-0001 “National Excellence Program” and European Social Fund in the framework of TA grant from Campus Hungary (Institute of Balassi).

References Aghajanzadeh, T.A., Reich, M., Kopriva, S., De Kok, L.J., 2018. Impact of chloride (NaCl, KCl) and sulphate (Na2SO4, K2SO4) salinity on glucosinolate metabolism in Brassica rapa. J. Agron. Crop Sci. 204 (2), 137 146. Ahmad, P., Alyemeni, M.N., Ahanger, M.A., Wijaya, L., Alam, P., Kumar, A., et al., 2018. Upregulation of antioxidant and gyloxalase systems mitigates NaCl stress in Brassica juncea by supplementation of zinc and calcium. J. Plant Interact. 13 (1), 151 162. Available from: https://doi.org/10.1080/17429145.2018.1441452.

Plant Life under Changing Environment

766

30. Role of metabolites in abiotic stress tolerance

Ahammed, G.J., Xu, W., Liu, A., Chen, S., 2019. Endogenous melatonin deficiency aggravates high temperatureinduced oxidative stress in Solanum lycopersicum L. Environ. Exp. Bot 161, 303 311. Available from: https:// doi.org/10.1016/j.envexpbot.2018.06.006. Akram, N.A., Shafiq, F., Ashraf, M., 2017. Ascorbic acid-a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front. Plant Sci. 8, 613. Alam, M.N., Zhang, L., Yang, L., Islam, M.R., Liu, Y., Luo, H., et al., 2018. Transcriptomic profiling of tall fescue in response to heat stress and improved thermotolerance by melatonin and 24-epibrassinolide. BMC Genomics 19, 224. Available from: https://doi.org/10.1186/s12864-018-4588-y. Amaˆncio, S., Gero´s, H., Dietz, K.J., Blumwald, E., 2017. The use of systems biology for enhancing crop abiotic stress tolerance. Front. Plant Sci. Annunziata, M.G., Ciarmiello, L.F., Woodrow, P., Maximova, E., Fuggi, A., Carillo, P., 2017. Durum wheat roots adapt to salinity remodeling the cellular content of nitrogen metabolites and sucrose. Front. Plant Sci. 7, 2035. Available from: https://doi.org/10.3389/fpls.2016.02035. Arnao, M.B., Herna´ndez-Ruiz, J., 2018. Melatonin and its relationship to plant hormones. Ann. Bot. 121, 195 207. Balfago´n, D., Zandalinas, S.I., Balin˜o, P., Muriach, M., Go´mez-Cadenas, A., 2018. Involvement of ascorbate peroxidase and heat shock proteins on citrus tolerance to combined conditions of drought and high temperatures. Plant Physiol. Biochem. 127, 194 199. Bartoli, C.G., Buet, A., Grozeff, G.G., Galatro, A., Simontacchi, M., 2017. Ascorbate-glutathione cycle and abiotic stress tolerance in plants. Ascorbic Acid in Plant Growth, Development and Stress Tolerance. Springer, Cham, pp. 177 200. Batth, R., Singh, K., Kumari, S., Mustafiz, A., 2017. Transcript profiling reveals the presence of abiotic stress and developmental stage specific ascorbate oxidase genes in plants. Front. Plant Sci. 8, 198. Benavides, M.P., Groppa, M.D., Recalde, L., Verstraeten, S.V., 2018. Effects of polyamines on cadmium- and copper-mediated alterations in wheat (Triticum aestivum L) and sunflower (Helianthus annuus L) seedling membrane fluidity. Arch. Biochem. Biophys. 654, 27 39. Bibbiani, S., Colzi, I., Taiti, C., Nissim, W.G., Papini, A., Mancuso, S., et al., 2018. Smelling the metal: volatile organic compound emission under Zn excess in the mint Tetradenia riparia. Plant Sci. Available from: https:// doi.org/10.1016/j.plantsci.2018.03.006. Borges, C.V., Minatel, I.O., Gomez-Gomez, H.A., Lima, G.P.P., 2017. Medicinal plants: influence of environmental factors on the content of secondary metabolites. In: Ghorbanpour, M., Varma, A. (Eds.), Medicinal Plants and Environmental Challenges. Springer, Cham. Byrt, C.S., Munns, R., Burton, R.A., Gilliham, M., Wege, S., 2018. Root cell wall solutions for crop plants in saline soils. Plant Sci. 269, 47 55. Cao, S., Du, X.H., Li, L.H., Liu, Y.D., Zhang, L., Pan, X., et al., 2017. Overexpression of Populus tomentosa cytosolic ascorbate peroxidase enhances abiotic stress tolerance in tobacco plants. Russ. J. Plant Physiol. 64 (2), 224 234. Carillo, P., 2018. GABA shunt in durum wheat. Front. Plant Sci. 9, 100. Available from: https://doi.org/10.3389/ fpls.2018.00100. Castiglioni, P., Bell, E., Lund, A., Rosenberg, A.F., Galligan, M., Hinchey, B.S., et al., 2018. Identification of GB1, a gene whose constitutive overexpression increases glycinebetaine content in maize and soybean. Plant Direct 2 (2), e00040. Chen, Z., Gu, Q., Yu, X., Huang, L., Xu, S., Wang, R., et al., 2018. Hydrogen peroxide acts downstream of melatonin to induce lateral root formation. Ann. Bot. 121 (6), 1127 1136. Cheng, B., Li, Z., Liang, L., Cao, Y., Zeng, W., Zhang, X., et al., 2018. The γ-aminobutyric acid (GABA) alleviates salt stress damage during seeds germination of white clover associated with Na1/K1 transportation, dehydrins accumulation, and stress-related genes expression in white clover. Int. J. Mol. Sci. 19 (9), 2520. Choudhury, F.K., Rivero, R.M., Blumwald, E., Mittler, R., 2017. Reactive oxygen species, abiotic stress and stress combination. Plant J. 90 (5), 856 867. Cocetta, G., Mishra, S., Raffaelli, A., Ferrante, A., 2018. Effect of heat root stress and high salinity on glucosinolates metabolism in wild rocket. J. Plant Physiol. 231, 261 270. Debnath, B., Hussain, M., Irshad, M., Mitra, S., Li, M., Liu, S., et al., 2018. Exogenous melatonin mitigates acid rain stress to tomato plants through modulation of leaf ultrastructure, photosynthesis and antioxidant potential. Molecules 23 (2), 388. Available from: https://doi.org/10.3390/molecules23020388.

Plant Life under Changing Environment

References

767

de Brito Francisco, R., Martinoia, E., 2018. The vacuolar transportome of plant specialized metabolites. Plant Cell Physiol. 59 (7), 1326 1336. Available from: https://doi.org/10.1093/pcp/pcy039. de Freitas, P.A.F., de Souza Miranda, R., Marques, E.C., Prisco, J.T., Gomes-Filho, E., 2018. Salt tolerance induced by exogenous proline in maize is related to low oxidative damage and favorable ionic homeostasis. J. Plant Growth Regul. 37, 911 924. De la Torre-Gonza´lez, A., Montesinos-pereira, D., Blasco, B., Ruiz, J.M., 2018. Influence of the proline metabolism and glycine betaine on tolerance to salt stress in tomato (Solanum lycopersicum L.) commercial genotypes. J. Plant Physiol. 231, 329 336. del Carmen Martı´nez-Ballesta, M., Moreno, D.A., Carvajal, M., 2013. The physiological importance of glucosinolates on plant response to abiotic stress in Brassica. Int. J. Mol. Sci. 14 (6), 11607 11625. Delorge, I., Janiak, M., Carpentier, S., Van Dijck, P., 2014. Fine tuning of trehalose biosynthesis and hydrolysis as novel tools for the generation of abiotic stress tolerant plants. Front. Plant Sci. 5, 147. Derakhshani, Z., Malherbe, F., Bhave, M., 2017. Multifunctional biomolecules with roles in abiotic stress tolerance as well as nutraceutical potential. J. Plant Biochem. Biotechnol. 26 (2), 121 131. Dumschott, K., Richter, A., Loescher, W., Merchant, A., 2017. Post photosynthetic carbon partitioning to sugar alcohols and consequences for plant growth. Phytochemistry 144, 243 252. Dumschott, K., Blessing, C.H., Merchant, A., 2018. Quantification of soluble metabolites and compound-specific δ13C in response to water availability and developmental stages in field grown chickpea (Cicer arietinum L.). Agronomy 8, 115. Available from: https://doi.org/10.3390/agronomy8070115. Dutta, T., Neelapu, N.R., Wani, S.H., Challa, S., 2018. Compatible solute engineering of crop plants for improved tolerance toward abiotic stresses. In: Wani, S.H. (Ed.), Biochemical, Physiological and Molecular Avenues for Combating Abiotic Stress Tolerance in Plants. Academic Press, Elsevier. pp. 221 254. Egert, A., Keller, F., Peters, S., 2013. Abiotic stress-induced accumulation of raffinose in Arabidopsis leaves is mediated by a single raffinose synthase (RS5, At5g40390). BMC Plant Biol. 13, 218. Erland, L.A., Saxena, P.K., 2018. Melatonin in plant morphogenesis. In Vitro Cell. Dev. Biol. Plant 54 (1), 3 24. Erland, L.A., Turi, C.E., Saxena, P.K., 2016. Serotonin: an ancient molecule and an important regulator of plant processes. Biotechnol. Adv. 34 (8), 1347 1361. Erland, L.A., Shukla, M.R., Singh, A.S., Murch, S.J., Saxena, P.K., 2018. Melatonin and serotonin: mediators in the symphony of plant morphogenesis. J. Pineal Res. 64 (2), e12452. Espasandin, F.D., Calzadilla, P.I., Maiale, S.J., Ruiz, O.A., Sansberro, P.A., 2018. Overexpression of the arginine decarboxylase gene improves tolerance to salt stress in Lotus tenuis plants. J. Plant Growth Regul. 37 (1), 156 165. Farooq, M., Nawaz, A., Chaudhry, M.A.M., Indrasti, R., Rehman, A., 2017. Improving resistance against terminal drought in bread wheat by exogenous application of proline and gamma-aminobutyric acid. J. Agron. Crop Sci. 203 (6), 464 472. Fazal, H., Abbasi, B.H., Ahmad, N., Ali, M., 2018. Exogenous melatonin trigger biomass accumulation and production of stress enzymes during callogenesis in medicinally important Prunella vulgaris L. (Selfheal). Physiol. Mol. Biol. Plants 1 9. Available from: https://doi.org/10.1007/s12298-018-0567-7. Ferchichi, S., Hessini, K., Dell’Aversana, E., D’Amelia, L., Woodrow, P., Ciarmiello, L.F., et al., 2018. Hordeum vulgare and Hordeum maritimum respond to extended salinity stress displaying different temporal accumulation pattern of metabolites. Funct. Plant Biol. 45, 1096 1109. Fichman, Y., Gerdes, S.Y., Kova´cs, H., Szabados, L., Zilberstein, A., Csonka, L.N., 2015. Evolution of proline biosynthesis: enzymology, bioinformatics, genetics, and transcriptional regulation. Biol. Rev. 90 (4), 1065 1099. Figueroa, C.M., Lunn, J.E., 2016. A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiol. 172, 7 27. Available from: https://doi.org/10.1104/pp.16.00417. Freitas, V.S., de Souza Miranda, R., Costa, J.H., de Oliveira, D.F., de Oliveira Paula, S., de Castro Miguel, E., et al., 2018. Ethylene triggers salt tolerance in maize genotypes by modulating polyamine catabolism enzymes associated with H2O2 production. Environ. Exp. Bot. 145, 75 86. Gangl, R., Tenhaken, R., 2016. Raffinose family oligosaccharides act as galactose stores in seeds and are required for rapid germination of Arabidopsis in the dark. Front. Plant Sci. 7, 1115. George, S., Manoharan, D., Li, J., Britton, M., Parida, A., 2017. Drought and salt stress in Chrysopogon zizanioides leads to common and specific transcriptomic responses and may affect essential oil composition and benzylisoquinoline alkaloids metabolism. Curr. Plant Biol. 11 12, 12 22.

Plant Life under Changing Environment

768

30. Role of metabolites in abiotic stress tolerance

George, S., Manoharan, D., Li, J., Britton, M., Parida, A., 2018. Drought and salt stress in Macrotyloma uniflorum leads to common and specific transcriptomic responses and reveals importance of raffinose family oligosaccharides in stress tolerance. Gene Rep. 10, 7 16. Gerszberg, A., Hnatuszko-Konka, K., 2017. Tomato tolerance to abiotic stress: a review of most often engineered target sequences. Plant Growth Regul. 83 (2), 175 198. Gong, X., Shi, S., Dou, F., Song, Y., Ma, F., 2017. Exogenous melatonin alleviates alkaline stress in Malus hupehensis Rehd. by regulating the biosynthesis of polyamines. Molecules 22 (9), 1542. Available from: https://doi.org/ 10.3390/molecules22091542. Goren, A., Ashlock, D., Tetlow, I.J., 2018. Starch formation inside plastids of higher plants. Protoplasma 255, 1855 1876. Govind, S.R., Jogaiah, S., Abdelrahman, M., Shetty, H.S., Tran, L.S.P., 2016. Exogenous trehalose treatment enhances the activities of defense-related enzymes and triggers resistance against downy mildew disease of pearl millet. Front. Plant Sci. 7, 1593. Available from: https://doi.org/10.3389/fpls.2016.01593. Graca, J., 2015. Suberin: the biopolyester at the frontier of plants. Front. Chem. 3, 62. Available from: https://doi. org/10.3389/fchem.2015.00062. Guo, Y.Y., Tian, S.S., Liu, S.S., Wang, W.Q., Sui, N., 2018. Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress. Photosynthetica 56, 861 872. Gupta, P., De, B., 2017. Metabolomics analysis of rice responses to salinity stress revealed elevation of serotonin, and gentisic acid levels in leaves of tolerant varieties. Plant Signal. Behav. 12 (7), e1335845. Han, B., Fu, L., Zhang, D., He, X., Chen, Q., Peng, M., et al., 2016. Interspecies and intraspecies analysis of trehalose contents and the biosynthesis pathway gene family reveals crucial roles of trehalose in osmotic-stress tolerance in Cassava. Int. J. Mol. Sci. 17, 1077. Available from: https://doi.org/10.3390/ijms17071077. Henry, C., Bledsoe, S.W., Griffiths, C.A., Kollman, A., Paul, M.J., Sakr, S., et al., 2015. Differential role for trehalose metabolism in salt-stressed maize. Plant Physiol. 169, 1072 1089. Available from: https://doi.org/10.1104/pp.15.00729. Herna´ndez-Ruiz, J., Arnao, M.B., 2018. Relationship of melatonin and salicylic acid in biotic/abiotic plant stress responses. Agronomy 8 (4), 33. Available from: https://doi.org/10.3390/agronomy8040033. Hildebrandt, T.M., 2018. Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response. Plant Mol. Biol. 98 (1 2), 121 135. Hisyam, B., Alam, M.A., Naimah, N., Jahan, M.S., 2017. Roles of glycinebetaine on antioxidants and gene function in rice plants under water stress. Asian J. Plant Sci. 16, 132 140. Hossain, M.A., Li, Z.G., Hoque, T.S., Burritt, D.J., Fujita, M., Munne´-Bosch, S., 2017. Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. Protoplasma 255, 399 412. Housley, T.L., Sims, I.M., Cairns, A.J., Pollock, C.J., 2017. Fructans as reserve carbohydrates in crop plants. Photoassimilate Distribution Plants and Crops Source-Sink Relationships. Routledge, pp. 117 204. Huang, X., Vincken, J.P., Visser, R.G.F., Trindade, L.M., 2018. Production of heterologous storage polysaccharides in potato plants. In: Ulvskov, P. (Ed.), Plant polysaccharides: biosynthesis and bioengineering. (Annual Plant Reviews) vol. 41, Chichester, UK, pp. 389 408. Available from: https://doi.org/10.1002/9781444391015. Hwang, O.J., Back, K., 2018. Melatonin is involved in skotomorphogenesis by regulating brassinosteroid biosynthesis in rice plants. J. Pineal Res. 65 (2). Available from: https://doi.org/10.1111/jpi.12495. Iba´n˜ez, C., Collada, C., Casado, R., Gonza´lez-Melendi, P., Aragoncillo, C., Allona, I., 2013. Winter induction of the galactinol synthase gene is associated with endodormancy in chestnut trees. Trees 27, 1309 13169. Ji, J., Yue, J., Xie, T., Chen, W., Du, C., Chang, E., et al., 2018. Roles of γ-aminobutyric acid on salinity-responsive genes at transcriptomic level in poplar: involving in abscisic acid and ethylene-signalling pathways. Planta 248, 675 690. Joshi, R., Singla-Pareek, S.L., Pareek, A., 2018. Engineering abiotic stress response in plants for biomass production. JBC ,http://www.jbc.org/cgi/doi/10.1074/jbc.TM117.000232.. Kaur, H., Mukherjee, S., Baluska, F., Bhatla, S.C., 2015. Regulatory roles of serotonin and melatonin in abiotic stress tolerance in plants. Plant Signal. Behav. 10 (11), e1049788. Kaya, C., Sonmez, O., Aydemir, S., Ashraf, M., Dikilitas, M., 2013. Exogenous application of mannitol and thiourea regulates plant growth and oxidative stress responses in salt-stressed maize (Zea mays L.). J. Plant Interact. 8 (3), 234 241. Kaya, C., Ashraf, M., Sonmez, O., 2018. Combination of nitric oxide and thiamin regulates oxidative defense machinery and key physiological parameters in salt-stressed plants of two maize cultivars differing in salinity tolerance. Adv. Agric. Sci. 6 (1), 34 44.

Plant Life under Changing Environment

References

769

¨ ner, E.T., 2018. Fructans of the saline world. Biotechnol. Adv. 36, Kirtel, O., Versluys, M., Van den Ende, W., O 1524 1539. Kito, K., Yamane, K., Yamamori, T., Matsuhira, H., Tanaka, Y., Takabe, T., 2018. Isolation, functional characterization and stress responses of raffinose synthase genes in sugar beet. J. Plant Biochem. Biotechnol. 27 (1), 36 45. Kosova´, K., Vı´ta´mva´s, P., Urban, M.O., Pra´sˇ il, I.T., Renaut, J., 2018. Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. Front. Plant Sci. 9, 122. Krasensky, J., Broyart, C., Rabanal, F.A., Jonak, C., 2014. The redox-sensitive chloroplast trehalose-6-phosphate AtTPPD regulates salt stress tolerance. Antiox. Redox Signal. 21 (9), 1289 1304. Kumar, Y., Prakash, O., Tripathi, H., Tandon, S., Gupta, M.M., Rahman, L.U., et al., 2018. AromaDb: a database of medicinal and aromatic plant’s aroma molecules with phytochemistry and therapeutic potentials. Front. Plant Sci. 9, 1081. Available from: https://doi.org/10.3389/fpls.2018.01081. Lee, K., Hwang, O.J., Reiter, R.J., Back, K., 2018. Flavonoids inhibit both rice and sheep serotonin N-acetyltransferases and reduce melatonin levels in plants. J. Pineal Res. 65, e12512. Li, Y., Fan, Y., Ma, Y., Zhang, Z., Yue, H., Wang, L., et al., 2017. Effects of exogenous γ-aminobutyric acid (GABA) on photosynthesis and antioxidant system in pepper (Capsicum annuum L.) seedlings under low light stress. J. Plant Growth Regul. 36 (2), 436 449. Li, S., Yang, Y., Zhang, Q., Liu, N., Xu, Q., Hu, L., 2018a. Differential physiological and metabolic response to low temperature in two zoysiagrass genotypes native to high and low latitude. PLoS One 13 (6), e0198885. Available from: https://doi.org/10.1371/journal.pone.0198885. Li, Z., Peng, Y., Huang, B., 2018b. Alteration of transcripts of stress-protective genes and transcriptional factors by γ-aminobutyric acid (GABA) associated with improved heat and drought tolerance in creeping bentgrass (Agrostis stolonifera). Int. J. Mol. Sci. 19 (6), 1623. Liang, B., Ma, C., Zhang, Z., Wei, Z., Gao, T., Zhao, Q., et al., 2018a. Long-term exogenous application of melatonin improves nutrient uptake fluxes in apple plants under moderate drought stress. Environ. Exp. Bot. 155, 650 661. Liang, D., Shen, Y., Ni, Z., Wang, Q., Lei, Z., Xu, N., et al., 2018b. Exogenous melatonin application delays senescence of kiwifruit leaves by regulating the antioxidant capacity and biosynthesis of flavonoids. Front. Plant Sci. 9, 426. Liao, J., Wu, X., Xing, Z., Li, Q., Duan, Y., Fang, W., et al., 2017. γ-Aminobutyric acid (GABA) accumulation in tea (Camellia sinensis L.) through the GABA shunt and polyamine degradation pathways under anoxia. J. Agric. Food. Chem. 65 (14), 3013 3018. Lin, Y., Zhang, J., Gao, W., Chen, Y., Li, H., Lawlor, D.W., et al., 2017. Exogenous trehalose improves growth under limiting nitrogen through upregulation of nitrogen metabolism. BMC Plant Biol. 17 (1), 247. Liu, N., Lin, S., Huang, B., 2017. Differential effects of glycine betaine and spermidine on osmotic adjustment and antioxidant defense contributing to improved drought tolerance in creeping bentgrass. J. Am. Soc. Hortic. Sci. 142 (1), 20 26. Liu, Y., Song, Y., Zeng, S., Patra, B., Yuan, L., Wang, Y., 2018a. Isolation and characterization of a salt stressresponsive betaine aldehyde dehydrogenase in Lycium ruthenicum Murr. Physiol. Plant. 163 (1), 73 87. Liu, F., Huang, N., Wang, L., Ling, H., Sun, T., Ahmad, W., et al., 2018b. A novel L-ascorbate peroxidase 6 gene, ScAPX6, plays an important role in the regulation of response to biotic and abiotic stresses in sugarcane. Front. Plant Sci. 8, 2262. Livingston, D.P., Hincha, D.K., Heyer, A.G., 2009. Fructan and its relationship to abiotic stress tolerance in plants. Cell. Mol. Life Sci. 66, 2007 2023. Available from: https://doi.org/10.1007/s00018-009-0002-x. Loescher, W.H., Everard, J.D., 2000. Regulation of sugar alcohol biosynthesis. Photosynthesis. Springer, Dordrecht, pp. 275 299. Lo´pez-Go´mez, M., Hidalgo-Castellanos, J., Mun˜oz-Sa´nchez, J.R., Marı´n-Pen˜a, A.J., Lluch, C., Herrera-Cervera, J. A., 2017. Polyamines contribute to salinity tolerance in the symbiosis Medicago truncatula-Sinorhizobium meliloti by preventing oxidative damage. Plant Physiol. Biochem. 116, 9 17. Lunn, J.E., Delorge, I., Figueroa, C.M., Van Dijck, P., Stitt, M., 2014. Trehalose metabolism in plants. Plant J. 79 (4), 544 567. Macknight, R.C., Laing, W.A., Bulley, S.M., Broad, R.C., Johnson, A.A., Hellens, R.P., 2017. Increasing ascorbate levels in crops to enhance human nutrition and plant abiotic stress tolerance. Curr. Opin. Biotechnol. 44, 153 160.

Plant Life under Changing Environment

770

30. Role of metabolites in abiotic stress tolerance

Mafu, S., Ding, Y., Murphy, K.M., Yaacoobi, O., Addison, B., Zerbe, P., 2018. Discovery, biosynthesis and stressrelated accumulation of dolabradiene-derived defenses in maize. Plant Physiol. 176, 2677 2690. Mahmud, J.A., Hasanuzzaman, M., Nahar, K., Rahman, A., Hossain, M.S., Fujita, M., 2017. γ-Aminobutyric acid (GABA) confers chromium stress tolerance in Brassica juncea L. by modulating the antioxidant defense and glyoxalase systems. Ecotoxicology 26 (5), 675 690. Mansour, M.M.F., 1998. Protection of plasma membrane of onion epidermal cells by glycinebetaine and proline against NaCl stress. Plant Physiol. Biochem. 36 (10), 767 772. Mansour, M.M.F., Ali, E.F., 2017. Glycinebetaine in saline conditions: an assessment of the current state of knowledge. Acta Physiol. Plant. 39 (2), 56. Martinez, V., Nieves-Cordones, M., Lopez-Delacalle, M., Rodenas, R., Mestre, T.C., Garcia-Sanchez, F., et al., 2018. Tolerance to stress combination in tomato plants: new insights in the protective role of melatonin. Molecules 23 (3), 535. McKinley, B.A., Casto, A.L., Rooney, W.L., Mullet, J.E., 2018. Developmental dynamics of stem starch accumulation in Sorghum bicolor. Plant Direct 1 15. Available from: https://doi.org/10.1002/pld3.74. Mertz, R.A., Brutnell, T.P., 2014. Bundle sheath suberization in grass leaves: multiple barriers to characterization. J. Exp. Bot. 65 (13), 3371 3380. Moles, T.M., Mariotti, L., De Pedro, L.F., Guglielminetti, L., Picciarelli, P., Scartazza, A., 2018. Drought induced changes of leaf-to-root relationships in two tomato genotypes. Plant Physiol. Biochem. 128, 24 31. Moradi, P., Ford-Lloyd, B., Pritchard, J., 2017. Metabolomic approach reveals the biochemical mechanisms underlying drought stress tolerance in thyme. Anal. Biochem. 527, 49 62. Moradi Peynevandi, K., Razavi, S.M., Zahri, S., 2018. The ameliorating effects of polyamine supplement on physiological and biochemical parameters of Stevia rebaudiana Bertoni under cold stress. Plant Prod. Sci. 21 (2), 123 131. Mostofa, M.G., Hossain, M.A., Fujita, M., 2015. Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma 252 (2), 461 475. Mukherjee, S., 2018. Novel perspectives on the molecular crosstalk mechanisms of serotonin and melatonin in plants. Plant Physiol. Biochem. 132, 33 45. Nishizawa, A., Yabuta, Y., Shigeoka, S., 2008. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251 1263. Nobukazu, S., 2016. Secondary metabolites in plants: transport and self-tolerance mechanisms. Biosci. Biotechnol. Biochem. 80 (7), 1283 1293. Available from: https://doi.org/10.1080/09168451.2016.1151344. Noman, A., Ali, Q., Naseem, J., Javed, M.T., Kanwal, H., Islam, W., et al., 2018. Sugar beet extract acts as a natural bio-stimulant for physio-biochemical attributes in water stressed wheat (Triticum aestivum L.). Acta Physiol. Plant. 40 (6), 110. Novakovi´c, L., Guo, T., Bacic, A., Sampathkumar, A., Johnson, K., 2018. Hitting the wall—sensing and signaling pathways involved in plant cell wall remodeling in response to abiotic stress. Plants 7 (4), 89. Oszvald, M., Primavesi, L.F., Griffiths, C.A., Cohn, J., Basu, S., Nuccio, M.L., et al., 2018. Trehalose-6-phosphate regulates photosynthesis and assimilate partitioning in reproductive tissue. Plant Physiol. Available from: https://doi.org/10.1104/pp.17.01673. Pa´l, M., Csa´va´s, G., Szalai, G., Ola´h, T., Khalil, R., Yordanova, R., et al., 2017. Polyamines may influence phytochelatin synthesis during Cd stress in rice. J. Hazard. Mater. 340, 272 280. Pa´l, M., Tajti, J., Szalai, G., Peeva, V., Ve´gh, B., Janda, T., 2018. Interaction of polyamines, abscisic acid and proline under osmotic stress in the leaves of wheat plants. Sci. Rep. 8 (1), 12839. Palliyaguru, D.L., Yuan, J.M., Kensler, T.W., Fahey, J.W., 2018. Isothiocyanates: translating the power of plants to people. Mol. Nutr. Food Res. 62, e1700965. Pandey, S., Fartyal, D., Agarwal, A., Shukla, T., James, D., Kaul, T., et al., 2017. Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front. Plant Sci. 8, 581. Per, T.S., Khan, N.A., Reddy, P.S., Masood, A., Hasanuzzaman, M., Khan, M.I.R., et al., 2017. Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics. Plant Physiol. Biochem. 115, 126 140. Phillips, K., Majola, A., Gokul, A., Keyster, M., Ludidi, N., Egbichi, I., 2018. Inhibition of NOS-like activity in maize alters the expression of genes involved in H2O2 scavenging and glycine betaine biosynthesis. Sci. Rep. 8 (1), 12628.

Plant Life under Changing Environment

References

771

Pommerrenig, B., Ludewig, F., Cvetkovic, J., Trentmann, O., Klemens, P.A.W., Neuhaus, H.E., 2018. In concert: orchestrated changes in carbohydrate homeostasis are critical for plant abiotic stress tolerance. Plant Cell Physiol. 59 (7), 1290 1299. Available from: https://doi.org/10.1093/pcp/pcy037. Qin, D., Zhao, C.L., Liu, X.Y., Wang, P.W., 2017. Transgenic soybeans expressing betaine aldehyde dehydrogenase from Atriplex canescens show increased drought tolerance. Plant Breed. 136 (5), 699 709. Rady, M.O., Semida, W.M., El-Mageed, T.A.A., Hemida, K.A., Rady, M.M., 2018. Up-regulation of antioxidative defense systems by glycine betaine foliar application in onion plants confer tolerance to salinity stress. Sci. Hortic. 240, 614 622. Rajaeian, S., Ehsanpour, A.A., Javadi, M., Shojaee, B., 2017. Ethanolamine induced modification in glycine betaine and proline metabolism in Nicotiana rustica under salt stress. Biol. Plant. 61 (4), 797 800. Ramakrishna, A., Ravinshankar, G.A., 2011. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal. Behav. 6 (11), 1720 1731. Rasheed, R., Iqbal, M., Ashraf, M.A., Hussain, I., Shafiq, F., Yousaf, A., et al., 2018. Glycine betaine counteracts the inhibitory effects of waterlogging on growth, photosynthetic pigments, oxidative defence system, nutrient composition, and fruit quality in tomato. J. Hortic. Sci. Biotechnol. 93 (4), 385 391. Rezaei-Chiyaneh, E., Seyyedi, S.M., Ebrahimian, E., Moghaddam, S.S., Damalas, C.A., 2018. Exogenous application of gamma-aminobutyric acid (GABA) alleviates the effect of water deficit stress in black cumin (Nigella sativa L.). Ind. Crops Prod. 112, 741 748. Razavi, F., Mahmoudi, R., Rabiei, V., Aghdam, M.S., Soleimani, A., 2018. Glycine betaine treatment attenuates chilling injury and maintains nutritional quality of hawthorn fruit during storage at low temperature. Sci. Hortic. 233, 188 194. Sabagh, A.E., Sorour, S., Ragab, A., Saneoka, H., Islam, M.S., 2017. The effect of exogenous application of proline and glycine betaineon the nodule activity of soybean under saline condition. J. Agric. Biotechnol. 2 (1), 1 5. Available from: https://doi.org/10.20936/JAB/170101. Savoi, S., Wong, D.C.J., Arapitsas, P., Miculan, M., Bucchetti, B., Peterlunger, E., et al., 2016. Transcriptome and metabolite profiling reveals that prolonged drought modulates the phenylpropanoid and terpenoid pathway in white grapes (Vitis vinifera L.). BMC Plant Biol. 16, 67. Available from: https://doi.org/10.1186/s12870-016-0760-1. Savvides, A., Ali, S., Tester, M., Fotopoulos, V., 2016. Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci. 21 (4), 329 340. Seki, M., Ohara, T., Hearn, T.J., Frank, A., Silva, V.C., Caldana, C., et al., 2017. Adjustment of the Arabidopsis circadian oscillator by sugar signalling dictates the regulation of starch metabolism. Sci. Rep. 7 (1), 8305. Selmar, D., Kleinwa¨chter, M., 2013. Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation of natural products. Plant Cell Physiol. 54 (6), 817 826. Available from: https://doi.org/10.1093/pcp/pct054. Semida, W.M., Hemida, K.A., Rady, M.M., 2018. Sequenced ascorbate-proline-glutathione seed treatment elevates cadmium tolerance in cucumber transplants. Ecotoxicol. Environ. Saf. 154, 171 179. Sengupta, M., Raychaudhuri, S.S., 2017. Partial alleviation of oxidative stress induced by gamma irradiation in Vigna radiata by polyamine treatment. Int. J. Radiat. Biol. 93 (8), 803 817. Sengupta, S., Mukherjee, S., Basak, P., Majumder, A.L., 2015. Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front. Plant Sci. 6, 656. Shanazari, M., Golkar, P., Mirmohammady Maibody, A.M., 2018. Effects of drought stress on some agronomic and bio-physiological traits of Triticum aestivum, Triticale, and Tritipyrum genotypes. Arch. Agron. Soil Sci. 64 (14), 2005 2018. Available from: https://doi.org/10.1080/03650340.2018.1472377. Sher, A., Hussain, S., Cai, L.J., Ahmad, M.I., Jamro, S.A., Rashid, A., 2017. Significance of chemical priming on yield and yield components of wheat under drought stress. Am. J. Plant Sci. 8 (06), 1339. Singer, S.D., Zou, J., Weselake, R.J., 2016. Abiotic factors influence plant storage lipid accumulation and composition. Plant Sci. 243, 1 9. Singh, A., Sharma, M.K., Sengar, R.S., 2017. Osmolytes: Proline metabolism in plants as sensors of abiotic stress. J. Appl. Nat. Sci. 9 (4), 2079 2092. Available from: https://doi.org/10.31018/jans.v9i4.1492. Singh, J., Singh, V., Sharma, P.C., 2018. Elucidating the role of osmotic, ionic and major salt responsive transcript components towards salinity tolerance in contrasting chickpea (Cicer arietinum L.) genotypes. Physiol. Mol. Biol. Plants 24 (3), 441 453.

Plant Life under Changing Environment

772

30. Role of metabolites in abiotic stress tolerance

Smeekens, S., 2015. From leaf to kernel: trehalose-6-phosphate signaling moves carbon in the field. Plant Physiol. 169, 912 913. Available from: https://doi.org/10.1104/pp.15.01177. Sun, X., Toma´sMatus, J., Chern Jan Wong, D., Wang, Z., Chai, F., Zhang, L., et al., 2018. The GARP/MYB-related grape transcription factor AQUILO improves cold tolerance and promotes the accumulation of raffinose family oligosaccharides. J. Exp. Bot. Available from: https://doi.org/10.1093/jxb/ery020. Suzuki, N., Rivero, R.M., Shulaev, V., Blumwald, E., Mittler, R., 2014. Abiotic and biotic stress combinations. New Phytol. 203, 32 43. Available from: https://doi.org/10.1111/nph.12797. Szalai, G., Janda, K., Darko´, E´., Janda, T., Peeva, V., Pa´l, M., 2017. Comparative analysis of polyamine metabolism in wheat and maize plants. Plant Physiol. Biochem. 112, 239 250. ´ ., Szoll ˝ osi, ˝ R., 2018. Mechanism of proline biosynthesis and role of proline metabolism enzymes under Szepesi, A environmental stress in plants. In: Plant Metabolites and Regulation Under Environmental Stress, pp. 337 353. Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., et al., 2002. Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. Cell Mol. Biol. 29, 417 426. Takahashi, Y., Tahara, M., Yamada, Y., Mitsudomi, Y., Koga, K., 2018. Characterization of the polyamine biosynthetic pathways and salt stress response in Brachypodium distachyon. J. Plant Growth Regul. 37 (2), 625 634. Tan, B.C., Lim, Y.S., Lau, S.E., 2017. Proteomics in commercial crops: an overview. J. Proteomics 169, 176 188. Tani, E., Sarri, E., Goufa, M., Asimakopoulou, G., Psychogiou, M., Bingham, E., et al., 2018. Seedling growth and transcriptional responses to salt shock and stress in Medicago sativa L., Medicago arborea L., and their hybrid (Alborea). Agronomy 8 (10), 231. ´ ., et al., 2010. Salicylic acid increased aldose reductase Tari, I., Kiss, G., Dee´r, A.K., Csisza´r, J., Erdei, L., Galle´, A activity and sorbitol accumulation in tomato plants under salt stress. Biol. Plant. 24 (4), 677 683. ´ ., 2015. The alleviation of the adverse effects of salt Tari, I., Csisza´r, J., Horva´th, E., Poo´r, P., Taka´cs, Z., Szepesi, A stress in the tomato plant by salicylic acid shows a time- and organ-specific antioxidant response. Acta Biol. Cracov. 57 (1), 21 30. Thalmann, M., Santelia, D., 2017. Starch as a determinant of plant fitness under abiotic stress. New Phytol. 214, 943 995. Available from: https://doi.org/10.1111/nph.14491. Tian, F., Wang, W., Liang, C., Wang, X., Wang, G., Wang, W., 2017. Overaccumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress. Crop J. 5 (1), 73 82. Tissier, A., 2018. Plant secretory structures: more than just reaction bags. Curr. Opin. Biotechnol. 49, 73 79. Urbancsok, J., Bones, A.M., Kissen, R., 2017. Glucosinolate-derived isothiocyanates inhibit Arabidopsis growth and the potency depends on their side chain structure. Int. J. Mol. Sci. 18 (11), 2372. Van den Ende, W., 2014. Sugars take a central position in plant growth, development and stress responses. A focus on apical dominance. Front. Plant Sci. 5, 313. Available from: https://doi.org/10.3389/flps.2014.00313. Van Oosten, M.J., Pepe, O., De Pascale, S., Silletti, S., Maggio, A., 2017. The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem. Biol. Technol. Agric. 4 (1), 5. Veenstra, L.D., Jannink, J.L., Sorrells, M.E., 2017. Wheat fructans: a potential breeding target for nutritionally improved, climate-resilient varieties. Crop Sci. 57 (3), 1624 1640. ¨ ner, E., Van den Ende, W., 2018. The fructan syndrome: evolutionary aspects Versluys, M., Kirtel, O., ToksoyO and common themes among plants and microbes. Plant Cell Environ. 41 (1), 16 38. Wan, J., Zhang, P., Sun, L., Li, S., Wang, R., Zhou, H., et al., 2018. Involvement of reactive oxygen species and auxin in serotonin-induced inhibition of primary root elongation. J. Plant Physiol. 229, 89 99. Wang, Cl, Zhang, S.C., Qi, S.D., Zheng, C.C., Wu, C.A., 2016. Delayed germination of Arabidopsis seeds under chilling stress by overexpressing an abiotic stress inducible GhTPS11. Gene 575, 206 212. Available from: https://doi.org/10.1016/j.gene.2015.08.056. Wang, Y., Reiter, R.J., Chan, Z., 2017. Phytomelatonin: a universal abiotic stress regulator. J. Exp. Bot. 69 (5), 963 974. Available from: https://doi.org/10.1093/jxb/erx473. Wang, X., Hou, L., Lu, Y., Wu, B., Gong, X., Liu, M., et al., 2018a. Metabolic adaptation of wheat grains contributes to a stable filling rate under heat stress. J. Exp. Bot. Available from: https://doi.org/10.1093/jxb/ ery303. Wang, Q., Zeng, S., Wu, X., Lei, H., Wang, Y., Tang, H., 2018b. Interspecies developmental differences in metabonomic phenotypes of Lycium ruthenicum and L. barbarum fruits. J. Proteome Res. 17 (9), 3223 3236.

Plant Life under Changing Environment

References

773

Wang, L., Shan, T., Xie, B., Ling, C., Shao, S., Jin, P., et al., 2019. Glycine betaine reduces chilling injury in peach fruit by enhancing phenolic and sugar metabolisms. Food Chem. 272, 530 538. Wei, D., Zhang, W., Wang, C., Meng, Q., Li, G., Chen, T.H., et al., 2017. Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants. Plant Sci. 257, 74 83. Wei, Z., Gao, T., Liang, B., Zhao, Q., Ma, F., Li, C., 2018. Effects of exogenous melatonin on methyl viologenmediated oxidative stress in apple leaf. Int. J. Mol. Sci. 19 (1), 316. Xalxo, R., Yadu, B., Chakraborty, P., Chandrakar, V., Keshavkant, S., 2017. Modulation of nickel toxicity by glycinebetaine and aspirin in Pennisetum typhoideum. Acta Biol. Szegediensis 61 (2), 163 171. Xie, D.W., Wang, X.N., Fu, L.S., Sun, J., Zheng, W., Li, Z.E., 2015. Identification of the trehalose-6-phosphate synthase gene family in winter wheat and expression analysis under conditions of freezing stress. J. Genet. 94 (1), 55 65. Xu, Z., Zhao, Y., Ge, Y., Peng, J., Dong, M., Yang, G., 2017a. Characterization of a vacuolar H1-ATPase G subunit gene from Juglans regia (JrVHAG1) involved in mannitol-induced osmotic stress tolerance. Plant Cell Rep. 36 (3), 407 418. Xu, Y., Wang, Y., Mattson, N., Yang, L., Jin, Q., 2017b. Genome-wide analysis of the Solanum tuberosum (potato) trehalose-6-phosphate synthase (TPS) gene family: evolution and differential expression during development and stress. BMC Genomics 18, 926. Available from: https://doi.org/10.1186/s12864-017-4298-x. Xu, Z., Sun, M., Jiang, X., Sun, H., Dang, X., Cong, H., et al., 2018. Glycinebetaine biosynthesis in response to osmotic stress depends on jasmonate signaling in watermelon suspension cells. Front. Plant Sci. 9, 1469. Available from: https://doi.org/10.3389/fpls.2018.01469. Xue, D., Zhang, X., Lu, X., Chen, G., Chen, Z.-H., 2017. Molecular and evolutionary mechanisms of cuticular wax for plant drought tolerance. Front. Plant Sci. 8, 621. Yadu, B., Chandrakar, V., Meena, R.K., Keshavkant, S., 2017. Glycinebetaine reduces oxidative injury and enhances fluoride stress tolerance via improving antioxidant enzymes, proline and genomic template stability in Cajanus cajan L. S. Afr. J. Bot. 111, 68 75. Yang, Y., Benning, C., 2018. Functions of triacylglycerols during plant development and stress. Curr. Opin. Biotechnol. 49, 191 198. Yao, W., Xu, T., Farooq, S.U., Jin, P., Zheng, Y., 2018. Glycine betaine treatment alleviates chilling injury in zucchini fruit (Cucurbita pepo L.) by modulating antioxidant enzymes and membrane fatty acid metabolism. Postharvest Biol. Technol. 144, 20 28. Yu, H.Q., Zhou, X.Y., Wang, Y.G., Zhou, S.F., Fu, F.L., Li, W.C., 2017. A betaine aldehyde dehydrogenase gene from Ammopiptanthus nanus enhances tolerance of Arabidopsis to high salt and drought stresses. Plant Growth Regul. 83 (2), 265 276. Yurchenko, O., Kimberlin, A., Mehling, M., Koo, A.J., Chapman, K.D., Mullen, R.T., et al., 2018. Response of high leaf-oil Arabidopsis thaliana plant lines to biotic or abiotic stress. Plant Signal. Behav. 13 (5), e1464361. Available from: https://doi.org/10.1080/15592324.2018.1464361. Zandalinas, S.I., Mittler, R., Balfago´n, D., Arbona, V., Go´mez-Cadenas, A., 2018. Plant adaptations to the combination of drought and high temperatures. Physiol. Plant. 162 (1), 2 12. Zali, A.G., Ehsanzadeh, P., Szumny, A., Matkowski, A., 2018. Genotype-specific response of Foeniculum vulgare grain yield and essential oil composition to proline treatment under different irrigation conditions. Ind. Crops Prod. 124, 177 185. Zapata, P.J., Serrano, M., Garcı´a-Legaz, M.F., Pretel, M.T., Botella, M.A., 2017. Short term effect of salt shock on ethylene and polyamines depends on plant salt sensitivity. Front. Plant Sci. 8, 855. Zarza, X., Atanasov, K.E., Marco, F., Arbona, V., Carrasco, P., Kopka, J., et al., 2017. Polyamine oxidase 5 loss-offunction mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. Plant Cell Environ. 40 (4), 527 542. Zechmann, B., 2018. Compartment-specific importance of ascorbate during environmental stress in plants. Antioxid. Redox Signal. 29 (15), 1488 1501. Zeng, L.D., Li, M., Chow, W.S., Peng, C.L., 2018. Susceptibility of an ascorbate-deficient mutant of Arabidopsis to high-light stress. Photosynthetica 56, 427. Available from: https://doi.org/10.1007/s11099-017-0759-3. Zhang, N., Zhang, H.J., Sun, Q.Q., Cao, Y.Y., Li, X., Zhao, B., et al., 2017. Proteomic analysis reveals a role of melatonin in promoting cucumber seed germination under high salinity by regulating energy production. Sci. Rep. 7, 503. Available from: https://doi.org/10.1038/s41598-017-00566-1.

Plant Life under Changing Environment

774

30. Role of metabolites in abiotic stress tolerance

Zhang, Q., Song, X., Bartels, D., 2018a. Sugar metabolism in the desiccation tolerant grass Oropetium thomaeum in response to environmental stresses. Plant Sci. 270, 30 36. Available from: https://doi.org/10.1016/j. plantsci.2018.02.004. Zhang, Y., Swart, C., Alseekh, S., Scossa, F., Jiang, L., Obata, T., et al., 2018b. The extra-pathway interactome of the TCA cycle: expected and unexpected metabolic interactions. Plant Physiol. Available from: https://doi. org/10.1104/pp.17.01687. Zouari, M., Elloumi, N., Labrousse, P., Rouina, B.B., Abdallah, F.B., Ahmed, C.B., 2018. Olive trees response to lead stress: exogenous proline provided better tolerance than glycine betaine. S. Afr. J. Bot. 118, 158 165.

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C H A P T E R

31 Role of melatonin and serotonin in plant stress tolerance Muhammad Adil1,2 and Byoung Ryong Jeong1,3,4 1

Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, Republic of Korea 2H.E.J. Research Institute of Chemistry-Biotechnology Wing, International Center for Chemical and Biological Sciences, University of Karachi, Karachi, Pakistan 3Department of Horticulture, Division of Applied Life Science Graduate School (BK 21 Plus program), Gyeongsang National University, Jinju, Republic of Korea 4Research Institute of Life Science, Gyeongsang National University, Jinju, Republic of Korea

31.1 Introduction Melatonin and serotonin are indoleamines chemically known as N-acetyl-o-methylserotonin and 5-hydroxytryptamine, respectively (Fig. 31.1). In animals the pineal gland and gut enterochromaffin cells, respectively, synthesize these indole group compounds. The excretion of melatonin from pineal gland strictly depends on light and is considered to be the key stimulus for its biosynthesis. The attention of biologists was drawn after the discovery of the melatonin by Lerner et al. (1958). The name melatonin was coined after its function as lightning the skin of reptiles, fish, and amphibians. However, after decades of research, it is known as a sleeping hormone that modulates mood, seasonal sexual behavior, immune system, and biological clock in animals including humans. While serotonin was first discovered by Dr. Erspamer in 1930 and named it enteramine due to its isolation from intestinal tracts of various animals; in 1948 it was renamed as serotonin after its structural study by Dr. Rapport at Cleveland Clinic, Ohio, United States. Afterward, this biomolecule was considered as a precursor for melatonin biosynthesis, and during the following years, it had been reported as a neurotransmitter, hormone, and mitogenic biochemical in animals. In addition, exogenous applications of serotonin in animals influence the intestinal motors and excretory functions to affect nutrient absorption and transportation.

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00034-5

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© 2020 Elsevier Inc. All rights reserved.

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31. Role of melatonin and serotonin in plant stress tolerance

FIGURE 31.1 Structures of ubiquitously found indole amines, melatonin and serotonin. (Structures source: PubChem).

In plants the history of these low-molecular weight compounds dates back to the mid20th century. Serotonin was first reported in Mucuna pruriens (L.) DC (cowhage) trichomes by Bowden at Leeds University, while his team was searching for the mechanism of pain in 1950 (Bowden et al., 1954). Since its discovery in plants, the major interest of the researchers was to produce phyto-serotonin in bulk for the pharmaceutical industry. However, interest in studying the role of these phyto-indoleamines in plant physiology increased, since the discovery of melatonin in plants by the independent research groups, Dubbels and Hattori in 1995 (Dubbels et al., 1995). Even earlier to these reports, melatonin was reported in dinoflagellate Gonyaulax polyedra and thereafter, it was recognized as a ubiquitous molecule found in animals, plants, and microbes. There is no absolute standard concentration of serotonin and melatonin as their concentrations vary among plant families, genus, cultivars, organs, and developmental stages (Paredes et al., 2009). Their concentrations also depend on environmental factors such as light and stress conditions. The hypothesis of Balzer and Hardeland (1996) geared the research on the role of melatonin in plants. They stipulated that phytomelatonin might act as chemical messengers of dark and light, a calmodulin biding factor, and free radical scavenger in plants. Also, they assumed that the melatonin/serotonin ratio in plants might control dark light responses, diurnal rhythms and seasonality (Balzer and Hardeland, 1996; Kolar et al., 1997). Thereafter, the confirmation of melatonin and serotonin in several plant species (Fig. 31.1) were put together to trace their functional roles in plants. For the purpose researchers exogenously applied them on plants and concluded their roles as a regulator of plant growth, photoperiodic rhythm, and seed germination (Posmyk and Janas, 2008). Zhang et al. (2014b)comprehensively reviewed the significance of phyto-melatonin in abiotic stress tolerance/resistance in plants, while Murch and Saxena’s (2002) review focuses on melatonin as a plant growth and development regulator. The recent review by Erland and Saxena (2017) enlightened the readers about the role of serotonin in plants. In this chapter we discuss the roles of two indolamines, phyto-serotonin and phyto-melatonin in plant stress physiology. Also will shed light on their biosynthesis in plants.

31.2 Tryptophan metabolism: biosynthesis of phyto-serotonin and melatonin Tryptophan, an amino acid and a precursor molecule for the biosynthesis of phytoserotonin and melatonin in animals, microbes, and plants. In animals, tryptophan is

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received from outside in their diets, while plants are specialized to synthesis it through a ubiquitous plant biosynthesis pathway. In the presence of anthranilate synthase an enzyme catalyzes the synthesis of anthranilate from a reaction between chorismite and glutamine. The subsequent phosphoryl-ribosylation and isomerization of N-(5-phosphoribosyl)-anthranilate produces indole-3-glycerol phosphate and then indole by indole-3-glycerol-phosphate lyase. The resulting indole is combined with L-serine to produce L-tryptophan in the presence of a tryptophan synthase complex. In plants the resulting tryptophan leads to biosynthesis of important indoleamines through four steps: decarboxylation, hydroxylation, N-acetylation, and O-methylation. These steps are catalyzed sequentially by four enzymes: (1) tryptophan decarboxylase (TDC), (2) tryptamine 5hydroxylase (T5H), (3) serotonin N-acetyltransferase (SNAT), and (4) N-acetylserotonin Omethyltransferase (ASMT). Back et al. (2016) suggested other four possible biosynthesis pathways for melatonin in plants due to the presence of two additional enzymes (tryptophan hydroxylase and caffeic acid O-methyltransferase) to abovementioned fours. They also suggested the localization of melatonin and its intermediates in different compartments of the plant cell (Back et al., 2016). Byeon et al. (2014) reported the expression of SNAT and ASMT in plant chloroplast and cytoplasm, respectively (Fig. 31.2). The TDC enzyme works as the major bottleneck in serotonin synthesis due to its low or negligible expression levels. The TDC was first cloned from Catharanthus roseus (De Luca et al., 1989) and further cloned in rice using a homology search (Kang et al., 2007).

FIGURE 31.2

Biosynthesis of serotonin and melatonin in plant cell: tryptophan is synthesized in chloroplast and transported to the ER for its conversion to serotonin. Four suggested intermediates for melatonin biosynthesis in plants are depicted in the figure. ER, endoplasmic reticulum. Source: Back, K., Tan, D.X., Reiter, R.J., 2016. Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J. Pineal Res. 61, 426 437; Byeon, Y., Lee, H.Y., Lee, K., Park, S., Back, K., 2014. Cellular localization and kinetics of the rice melatonin biosynthetic enzymes SNAT and ASMT. J. Pineal Res. 56, 107 114; Plant Metabolic Network database.

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Successful hydroxylation step occurs in the presence of molecular oxygen and requires tetrahydrobiopterin as a cofactor, while T5H constitutively expressed in healthy Oryza sativa (Kang et al., 2007). Compared to TDC, T5H has a higher enzyme activity with a lower Km value of 20 µM to tryptophan as a substrate (Kang et al., 2008). It is worthy to mention that tryptophan also serve as precursor for auxins (IAA; indole3-acetic acid, indole-3-butyric acid and p-hydroxyphenylacetic acid) synthesis (Murch et al., 2000; Ludwig-Mu¨ller and Cohen, 2002). The auxin IAA is synthesized via tryptophan-dependent and -intendent pathways. The intermediate products of tryptophan-dependent pathways are (1) indole-3-pyruvic acid and indole-3-acetaldehyde, (2) indole-3-acetamide, and (3) indole-3-acetonitrile (Normanly and Bartelt, 1999). Though Murch and Saxena (2002) proposed additional pathway to synthesize of IAA from an intermediate, tryptamine catalyzed by tryptamine deaminase is also directly connected to serotonin and melatonin biosynthesis (Murch and Saxena, 2002).

31.3 Fate of melatonin and serotonin in plants Since the discovery of melatonin in plants, researchers paid more attention to its biosynthesis in plants. Little is known about its ultimate fate after synthesis. However, in animals, it is well studied, and its fate can be determined from the hydroxylation reaction followed by conjugation with sulfate and glucuronic acid for final excretion (Kopin et al., 1961). The major difference of melatonin metabolism in plants is the hydroxylation position. In animals, hydroxylation at position 4, 5, or 6 is reported by cytochrome P450 enzyme (Ma et al., 2005), while in plants 2-hydroxymelatonin is the predominant product of melatonin metabolism which is catalyzed by the enzyme melatonin-2-hydroxylase (M2H) (Byeon et al., 2015b). In plants, four independent genes, for example, 2-ODD11, 2-ODD19, 2-ODD21, and 2-ODD33, encode the enzymes for melatonin catabolism to 2-hydroxymelatonin (Byeon et al., 2015a). These enzymes are mostly involved in the conversion of melatonin to 2-hydroxymelatonin and that is why 4 or 6-hydroxymelatonin never been detected in plants. Alternatively, melatonin is metabolized via the kynurenine pathway (Posmyk and Janas, 2008). In this route a melatonin side chain is first cyclogenesised to form cyclic 3-hydroxy-melatonin (C2OHM) by the action of free radical. The C2OHM is then converted to a N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) metabolite by cleaving the pyrrole ring in the structure (Tan et al., 2007b). Though AFMK can be obtained directly from a melatonin molecule via series of oxidation reactions, it is catabolized via pseudo-enzymes in the cells. This AFMK pathway is a potential route to detoxify at least 10 reactive oxygen species (ROS) and is believed to be the possible explanation for antioxidant properties of melatonin. Such pathway was studied in Eichornia crassipes (water hyacinth) and stipulated for higher antioxidant capacities than melatonin (Tan et al., 2007b). Serotonin is a precursor other than for melatonin biosynthesis; it produces several other derivatives that play important roles in plant defense against various stresses (Kang et al., 2009). These derivatives mainly include feruloylserotonin, 4-coumaroylserotonin, caffeoylserotonin, sinapoyl serotonin, and cinnamoylserotonin which belong to a phenylpropanoid amides (PAs) class of metabolites (Kang et al., 2009). These derivatives are synthesized by a condensation reaction of serotonin and cinnamoyl-CoA thioesters. An enzyme, serotonin Plant Life under Changing Environment

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N-hydroxycinnamoyltransferase, plays a terminal role in synthesis of PAs in cytosol (Tanaka et al., 2003). These PAs have been identified in more than 16 plant species of 8 different families.

31.4 Plant stress physiology and role of indolamines The study of plant responses to stresses is known as plant stress physiology. It is a series of biochemical processes taking place in plants to thrive harsh or stress conditions. Rhodes and Nadolska-Orczyk (2001) defined stress as an external factor/stimulus that adversely affects plant growth, productivity, reproductive capacity, or survival. There are several factors which are mostly categorized into two factors, biotic or biological and abiotic or environmental (Rhodes and Nadolska-Orczyk, 2001). Abiotic stress factors can be subdivided into chemical (salt, nutrients deficiency, other pollutants, etc.), mechanical (hardness of soil, hail, wind, etc.), and environmental (light, temperature, humidity, etc.), while biotic stresses are caused by bacteria, fungi, and viruses. To cope with these stress conditions, plants have specialized mechanical structures as the first line of defense, while for interaction/detection and adoption, plants produce signaling molecules to perceive stress and modulate cellular metabolic machinery accordingly. These signaling molecules are diverse in structure and function and act as ligands that bind to specific receptors. Structurally, these may range from simple gases (e.g., ethylene) to complex proteins. While melatonin and serotonin are structurally related to tryptophan and its precursors, they have been found at higher levels in plants which are exposed to harsh environments. The endogenous increase or exogenous application improves plant tolerance to stress conditions. Hence, here in this chapter, we discussed the roles of melatonin and serotonin in different individual stress conditions.

31.4.1 Environmental stresses 31.4.1.1 Temperature stress Plants are evolutionary flexed to tolerate and able to withstand with the swift temperature changes during the 24 hours day length. The oscillation in temperature during 24 hours is known as a diurnal (day/night) variation in air temperature and plays an important role in plants as it influences the photorespiration, which in turn influences the physiology, reproduction, and maturity of crops. For instance a plant in high desserts thrives at about 50 C during the day, while the temperature during the night falls to freezing levels. However, for plants in temperate and tropical zones, the fluctuation is less intense, but still the changes of 10 C 15 C over a day or a week are plausible. This necessitates a strong homeostasis mechanism in plants to thrive. However, there are additional anatomical features in plants that make them distinct over others to survive and limit the plant distribution in a local temperature regime. The detailed study of plant homeostasis is always of interest to plant biologists as global warming is a hot issue of concern for the future of this world.

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Temperature-related stresses are classed into three types: high, chilling, and freezing. These stresses in plants cause low germination rates, retarded growth, reduced photosynthesis, and often death due to the impaired metabolisms and altered redox state of the plant cell (Bita and Gerats, 2013). In addition, influence of temperature is most prominent on plant reproduction that compromises its productivity and yield (Hatfield and Prueger, 2015). For survival plants manifest different mechanisms to combat extreme temperature conditions and, for instance, long-term evolutionary adaptations at morphological and phenological levels, membrane lipid composition changes, leaf orientation and transpiration cooling, or short-term avoidance or acclimation are the mechanisms (Bita and Gerats, 2013; Larkindale and Vierling, 2008; Wahid et al., 2007). Other than these, internal antioxidant enzymes also play important roles in plant-cell hemostasis. Under higher temperatures, accelerated transcription and translation of heat shock proteins (HSPs) (Zou et al., 2009), production of phytohormones, such as abscisic acid (ABA), and antioxidant and other protective molecules (Maestri et al., 2002) are thought to be important for tolerance in plants. The basic line of defense against temperature stress in plants is thought to be the accumulation of compatible osmolytes, such as proline, glycine, betaine and soluble sugars, and cellular water balance, membrane stability, and osmotic adjustment (Sakamoto and Murata, 2002). In addition, alpha-tocopherol of leaves (vitamin E) plays an important role in cold acclimation and maintenance of redox homeostasis (Awasthi et al., 2015). The accumulation of cryoprotectants, such as soluble sugars, sugar alcohols, and nitrogenous compounds, also adds cold stress tolerance in plants (Janska´ et al., 2010). It is a well-established fact that during stress conditions, endogenously melatonin and serotonin levels in plants increases (Byeon and Back, 2014). This increase complements plant tolerance to stress conditions and help plants to thrive. In cold stress the melatonininduced tolerance can be explained from the upregulation of C-repeat-binding factors/ drought response element binding 1 factors (CBFs/DREBs) C-repeat binding factors, COR15a (cold responsive gene), CAMTA1 (freeze and drought tolerance genes), and ROSrelated antioxidant genes (ZAT10 and ZAT12) (Shi et al., 2014). In another study the application of melatonin to wheat seedlings showed an increase in antioxidant enzymes SOD, GPX, APX, and GR too and helped to improve growth and reduced oxidative damages (Turk et al., 2014). In addition the antioxidizing role of melatonin itself cannot be sidelined in this context. In heat stress, increased tolerance of the photosynthetic apparatus is an important factor to make plants viable (Hemantaranjan et al., 2014). It is well studied that elevated temperature causes malfunction of the photosystem (PS) II, which hinders the electron transport, and also increased ROS production with a prolonged exposure to heat stress. Higher ROS productions in plants also affect mitochondria and cause DNA damages and lipid peroxidation of the lipid membranes. The site (chloroplast) of melatonin synthesis makes it a key defender in the process of heat tolerance. However, melatonin synthesis in mitochondria is also reported in plants and may be the possible explanation for its role in heat tolerance (Wang et al., 2017). This synthesis occurs in a wider range of temperatures from 5 C to 75 C which makes it to sense that melatonin could be the first line of defense during heat stress. However, the heat tolerance cannot be solely speculated to melatonin, and the

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tolerance mechanism works in coordination with other protecting agents, such as antioxidant enzymes and phenols (Wahid et al., 2007). In addition, it is reported that melatonin protects cellular proteins and increases the expression of HSPs and helps to ameliorate the heat-induced photoinhibition and electrolyte leakage in tomato plants (Xu et al., 2016). Exogenously applied melatonin has also been found in upregulation of ion channel genes NHX1 and ATX1 (Li et al., 2012) and inhibition of cold-induced apoptosis through polyamines (Lei et al., 2004). 31.4.1.2 Water stress Among several stress factors in plants, water stress is considered of major importance as all biological processes occurring in plants need water. The term water stress mostly is used to indicate the deficiency of water and also is known as drought stress. However, excessive water or flooding causes waterlogging, a condition that leads to an anaerobic condition in roots and in surroundings. Plants cope with these two different conditions differently, that is, in drought condition, plants stop leaf growth and close the stomata to stop transpiration. In addition, in such condition, plants produce longer tap roots to get access to the water table at a distance. Drought is caused by two factors: presence of excessive solutes (salinity) and high temperature accompanied with lower rainfall and unavailability of water. In waterlogged condition, plants produce adventitious roots and aerenchyma tissues to accumulate air in the tissues to overcome the effect of anoxia. In both conditions the major threat to plants is water deficiency which affects the plants at all levels from molecular, cellular, and organ to the whole plant (Muscolo et al., 2015). The detailed information regarding plant responses to these conditions can be found in the previously published reviews (Kar, 2011; Nishiuchi et al., 2012; Osakabe et al., 2014). Melatonin and serotonin have been found effective against several stresses in plants and the mechanism of this is in ROS hunting. The increased ROS production during the drought and waterlogged conditions has been reported in plants and believed to be notorious for plant survival (Cruz de Carvalho, 2008). There are different kinds of ROS, mainly superoxide anion (O•22), hydrogen peroxide (H2O2), hydroxyl radical (•OH), singlet oxygen (1O2), peroxynitrite anion (ONOO2), and nitric oxide (NO). And melatonin, an amphiphilic compound, has the potential to eradicate all these from cells (Tan et al., 2013). In a study of Zheng et al. (2017), melatonin irrigation to roots or spray on leaves was effective to overcome the waterlogging stress in apple (Malus baccata) seedlings (Zheng et al., 2017). They observed a significant decrease in leaf chlorosis due to waterlogging stress. Their further investigation reported a significant increase in the endogenous melatonin synthesis during the waterlogging stress condition. Waterlogging stress suppresses the antioxidant enzymes. However, supplementation of exogenous melatonin has been proven helpful to revive their activities (Zheng et al., 2017). In addition the nutrient deficiency during waterlogging condition due to anoxia is the primary cause of loses in plant growth (Steffens et al., 2005). In management to this, Li et al. (2016a) found melatonin to buffer the nutrient deficiency (e.g., K and Na) effectively. The role of melatonin in drought stress is well studied in several plants including a model plant Arabidopsis. The greater antioxidant capacity and the amphiphilic nature of

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melatonin make it ideal to manage drought stress in plants. However, still the field trials are lacking in this context, while studies in glasshouse or in vitro are increasing each day. The major conclusion, increase in endogenous melatonin and serotonin levels in plants argued that these indole amines plays potential role in plant stress management. In Medicago sativa plants, root priming with melatonin significantly reduced malondialdehyde (MDA), H2O2, and NO levels during prolonged exposure to drought (Antoniou et al., 2017). The mechanism behind drought stress is believed to be the upregulation of MdCYP707A1, an ABA catabolic gene, and downregulation of MdNCED3, an ABA synthesis gene, to reduce ABA levels during the drought stress. Similarly, a prolonged exogenous application of melatonin delayed leaf senescence in apple (Wang et al., 2012). Also, the transgenic Arabidopsis carrying MzASMT genes to over express melatonin synthesis conferred resistance to drought and pathogens [27,28] (Zuo et al., 2014). 31.4.1.3 UV stress Due to increasing greenhouse-gas emission, the ozone layer depletion has risked our environment. This ozone layer in stratosphere filters the UV radiation coming from the sun and protects this biosphere from their harmful effects. The radiations oozing out of the protective layer have been proven lethal for all living organisms and are mainly divided into three main types, UV-A, UV-B, and UV-C. These radiations, mostly UV-B, have been implicated to inflict damages to the photosynthetic apparatus of green plants. The UV-B radiation affects the activity and content of Rubisco enzyme in leaf. Some have also reported its effect on photosynthetic pigments, stomatal conductance, and leaf and canopy morphology. The UV-A radiation is believed to be less deleterious to plants then UV-B in term of DNA damage and other as these radiations are in abundance (about 95%) near the equator (Verdaguer et al., 2017). However, prolonged exposure to solar UV radiations affects the PS II complex, Mn-cluster of the water-oxidizing complex, and D1 and D2 protein subunits (Verdaguer et al., 2017). In compensation, plants produce photoprotective compounds, such as phenolics and antioxidative enzymes, and melatonin to reduce the photooxidative stress (Afreen et al., 2006; Hardeland, 2016). Elevated levels of melatonin and serotonin in plants after stress treatment give the lead to its role in stress tolerance. The observation of higher melatonin contents in the Alpine and Mediterranean plants due to UV exposure also emphasizes the potential role of phyto-melatonin in UV-stress tolerance in plants (Tettamanti et al., 2000). This was further confirmed by Zhang et al. (2012) in transgenic Nicotiana sylvestris carrying human SNAT and hydroxyindole-O-methyl transferase (HIOMT) enzymes for overproduction of melatonin and exerted resistance against UV-B radiation-induced DNA damages (Zhang et al., 2012). In field condition the multivariate conditions, such as day length, UV irradiance, and water level, make the melatonin as a direct antioxidant and also as a trigger for the cross talks between plant growth regulators (PGRs) and stress environment (Arnao and Herna´ndez-Ruiz, 2014). Other than the toxic effects of incoming UV radiation, it also plays an important role in photomorphogenesis, and it has been considered as an option to enhance resistance against pests and diseases (Bornman et al., 2015). As a strategy, the synergistic application of UV radiation and melatonin/serotonin would help to increase the crop yield and to reduce the use of expensive and toxic pesticides.

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31.4.2 Chemical stress 31.4.2.1 Heavy metal stress Contamination by heavy metals around the world is increasing with an alarming rate and causing toxicity in plants (Eapen and D’souza, 2005; Kavamura and Esposito, 2010; Miransari, 2011). The d-block 53 elements of periodic table, having their density .5 g/cm3, are considered “heavy metals” (Ja¨rup, 2003). Plants utilize some of the essential heavy metals, such as Zn, Cu, Mn, Fe, Mo, B, Ni, Co, and B, for their normal physiological processes and growth and development, but in minute amounts. However, some metals, such as Hg, Cd, Pd, Al, and Cr, are nonessential and not required for plants and are toxic even in lower concentrations (Fidalgo et al., 2013; Gill et al., 2013). These nonessential heavy metals have hazardous effect on plants and cause reduction in plant growth and biomass accumulation. These effects are due to the altered plant physiological functions such as lower photosynthesis, water and nutrients imbalance, and senescence which leads to plant death (Singh et al., 2015). As a defense, plant cell membranes serve as the crucial checkpoints for an entrance of undesirable affluences into the cell. So, in other word, the membrane integrity is of utmost importance to combat the heavy metal toxicities. Once that enters the plant cell, it causes a significant decline in carotenoids and chlorophyll levels that lowers the level of PS II. Apart from these, CO2 assimilation also decreases as heavy metals react with the thiol group of RuBisCO and decrease its carboxylase activity in plants. Heavy metals also affect nitrate and ammonia fixation by interfering with functioning of the nitrate reductase/nitrite reductase and glutamine synthase, respectively (Hernandez et al., 1997; Lea and Miflin, 2003). In addition, toxicity by heavy metals also alters the endogenous hormonal balance by changing the transcription of plant hormone synthesis genes. In the case of metallophytes a well-organized system of metal uptake, translocation, and sequestration exists to make their living in heavy metal-polluted areas. Unlike the hyperaccumulating plants, nonhyperaccumulating plants do not translocate the heavy metals to aerial parts of the plants. This accumulation in roots leads to production of ROS and becomes deleterious to plants when ROS accumulation exceeds its scavenging (Mittler et al., 2004). This increased turnover of ROS in plant cells creates a series of disturbance in lipids, pigments, proteins, DNA, and other essential cellular molecules that causes even death of cells (Hossain et al., 2012a, 2012b; Mittler, 2002; Sharma and Dietz, 2009). Lee et al (2017) reported a twofold increase in melatonin synthesis in Cd-treated green macroalgae and stipulated the role of melatonin in Cd toxicity mitigation (Lee et al., 2017). Afterward, Gu et al. (2017) observed an increase in an endogenous level of melatonin in transgenic Arabidopsis roots and showed that a resistance to Cd stress with a decrease in a ROS level (Gu et al., 2017). This study was in support to the previously reported Cd tolerance in rice and tomato (Byeon et al., 2015a; Cai et al., 2017; Hasan et al., 2015b; Li et al., 2016b). These reports drove scientists to test melatonin for enhancing or increasing the tolerance in metallophytes to clean contaminated soil. The idea was tested by Tan et al. (2007a) who observed an increased tolerance of pea plants grown in soil contained with a heavy metal, Cu, and melatonin. Hasan et al. (2015a) correlated the melatonin-induced Cd stress mitigation in tomato plants to increased activities of antioxidant enzymes, H1ATPase, glutathione, and phytochelatins. A recent study by Tang et al. (2018) observed a

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68% increase in Cd accumulation when 100 µmol3/L melatonin was sprayed on Galinsoga parviflora plant, a hyperaccumulator plant. Galano et al. (2015) hypothesized the melatonin chelation property to reduce the metal-induced toxicity in cells. In this context, transgenic rice plants carrying overexpressed N-acetyltransferase 1 gene conferred resistance to Cd and showed an increase in grain yield. 31.4.2.2 Salinity stress Like other stresses, salinity also compromises the quality and quantity of agriculture crops. The continuous anthropogenic activities deter crops and food supply to the growing population of the world. High concentrations of salts in the soil affect plants by ionic pressure and osmotic stress (Zhu, 2002). However, effort of plant breeders eluded the effects by creating salt-tolerant cultivars. Additional effort with the advent of plant molecular biology using the genes responsible for salt tolerance and transgenic lines in several crops ensured crops for salt-affected soils. However, the in-depth studies of salt-stress tolerance in plants found the involvement of more than one gene in the tolerance mechanism. The ultimate tool box for the regulation of these multiple genes was found to be transcription factors (TFs). The TFs have been proven to be important to breed crops to be stress tolerant as they have the potential to regulate different stress-responsive genes. These TFs, including AP2/ERF, bZIP, NAC, MYB, and WRKY, were surmised in a short review (Kumar et al., 2017). There are additional strategies other than breeding which have been proven helpful to overcome the salinity stress. Among these selection of tolerant genotypes, inoculation of plant growth-promoting arbuscular mycorrhiza and or rhizobacteria, exogenous application of PGRs and osmoprotectants, seeds priming, and nutrients managements have also been proven helpful in salinity stress management (Farooq et al., 2017). Recent detection of human neurotransmitters, melatonin and serotonin in plants, and their alleviated levels with stress conditions have urged the role of the compounds in plant stress tolerance and management (Arnao and Herna´ndez-Ruiz, 2009; Mukherjee et al., 2014). Serotonin, a precursor molecule for melatonin, has been less studied in plant stress, while melatonin has been widely applied exogenously to manage plant stress. For instance, Li et al. (2012) and Mukherjee et al. (2014) exogenously applied melatonin to enhance stress tolerance of Malus hupehensis and Helianthus annuus, respectively. This enhanced tolerance is linked with a melatonin’s protective role in leaf chlorophyll and delayed senescence and preserves the efficiency of PS II (Park and Back, 2012; Wang et al., 2012, 2013). In addition, osmotic stress regulation and redox oxidative stress hemostasis are additional explanations for melatonin’s functional roles in salinity-stress management (Zheng et al., 2017). A study of Li et al. (2017) on watermelon found that melatonin alleviated the NaCl-induced decrease in photosynthetic rate and oxidative stress in a dosedependent manner. They linked the enhanced photosynthesis with inhibition of stomatal closure, improved light energy absorption, and electron transport in PS II. Similarly, Zhang et al. (2014a) reported enhanced germination of cucumber (Cucumis sativus L.) seeds with melatonin pretreatment under salinity stress. Their work suggested that increased expression of antioxidant enzymes and downregulation of ABA synthesis in melatoninpretreated seeds. In addition, others have reported salinity tolerance in Vicia faba L., O. sativa L., Citrus aurantium L., and Cynodon dactylon L. (Dawood and El-Awadi, 2015;

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Kostopoulou et al., 2015; Liang et al., 2015; Shi et al., 2014). Work by Chen et al. (2017) is worthy to mention here as their work on mutant Arabidopsis signified the role of endogenous melatonin in salinity stress tolerance. This study was in support of the reported salinity stress susceptibility in SNAT or ASMT mutant rice seedlings (Byeon and Back, 2016).

31.4.3 Biological stress The stress condition caused by viruses, bacteria, fungi, and herbivores are known as biological or biotech stress. Like other stresses in plants, plants have an intricate mechanism to defend themselves from these invaders. Plant cells have pattern-recognition receptors (PRRs) which help to recognize the evolutionarily conserved pathogen-associated molecular patterns (PAMPs) or microbe-associated molecular patterns (Nicaise et al., 2009). This perception evokes an immune response in plants, and this is called the PAMPtriggered immunity (PTI). On the other side an evolved resistant plant pathogen exerts to produce a virulence effecter protein to inhibit PTI, while defendant plants produce a resistance (R) protein to evoke effector-triggered immunity (Ponce de Leo´n and Montesano, 2013). These pathways stimulate downstream immune responses such as activation of multiple signaling pathways and transcription of specific genes that controls the pathogen proliferation and/or disease symptom expression. In addition, secondary metabolites (phenols, alkaloids, and saponin) and defense hormones (melatonin, serotonin, salicylic acid, ethylene, and jasmonic acid) are also produced in plants to boost the immunity (Alvarez et al., 2016; Zipfel, 2009). The adequate food supply to the world’s growing population is at risk due to various crop diseases. To control plants from pathogenesis, plant biologists have introduced different chemicals, such as pesticides and fungicides, and resistant varieties. These methods have been proven beneficial in a green revolution, but the excessive use of toxic chemicals has stacked our environment. Melatonin and serotonin are thought to be the promising alternatives to control pathogenesis in plants. Studies have confirmed antimicrobial activities of melatonin and serotonin in vitro. A comprehensive review by Erland and Saxena (2017) describes the detail function of serotonin in plant development, growth, and environmental stress regulation. They also explained the possible functional roles of serotonin during the damages caused by phytophagous insects and discussed the deleterious effects of serotonin on insects. Serotonin is thought to be involved in pathogen-specific resistance and also be involved in several downstream processes of plant defense. An increase in a leaf serotonin level was observed with the fungal (Bipolaris oryzae) pathogenesis in rice leaves and hindered the growth of fungal hyphae in leaf tissues (Ishihara et al., 2008b). In the same study an increased anthranilate synthase activity confirmed elevated levels of tryptophan-derivatives, that is, serotonin in rice plants in response to fungal infestation. An increase in a serotonin peroxidase activity and serotonin deposition in cell wall were also linked to pathogen resistance in wheat and rice plants (Ishihara et al., 2008b). The publicly available rice transcriptomic datasets (RiceCyc) also showed that induction of serotonin biosynthesis involves taxonomically diverse pathogens and also a diurnal regulation (Dharmawardhana et al., 2013). Melatonin, the end product of the serotonin metabolism is more prevalent in plants and has been studied widely. The increased endogenous melatonin level in Arabidopsis was

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observed upon infestation by Pseudomonas syringae pv. tomato (Shi et al., 2015). This increase was speculated to exert resistance in plants against pathogens (Ishihara et al., 2008a). Generally, it is believed that melatonin during fungal infection improves damages caused by diseases, reduces lesions, and inhibits pathogen expansion (Yin et al., 2013). The same occurred in Lupinus albus seeds infected with Penicillium spp., and an overexpression of pathogenesis-related genes were observed. Melatonin deficient (SNAT knockout) mutant reduces the melatonin level and increase the plant susceptibility to the pathogen (Lee Hyoung et al., 2015; Zhang et al., 2017). Studies have suggested the involvement of melatonin in the plant innate immunity, thickening of cell wall by accumulating cellulose, galactose, xylose, and callose to prevent pathogen infection (Qian et al., 2015).

31.5 Conclusion Stresses to plants are of concern as world crop productivity is constrained by stresses by different environmental factors. For management of these, different agrochemicals have been introduced to the market to help plants to withstand the environmental cues. These chemicals have also been proven toxic to the environment and our own health, and stringent regulations have been brought to control overuse and also to protect our environment. Since then, scientist started looking looked for alternatives, which will be safer and potent to assist or improve growth and productivity of crops. In this context, serotonin and melatonin seem to be promising as they have diverse ranges of physiological activities against plant stresses. Serotonin is a precursor for the melatonin synthesis in plants and has been not a focus for plant scientists in plant physiology. Both have proven their roles in delaying senescence, increase in plant biomass, plant organogenesis, inflorescence development, seed germination, and modulation of biotic and abiotic stresses. Studies on the roles of phyto-serotonin and phyto-melatonin in plants have implicated new ways of their use in plant stress management. However, still more work needs to be done on their formulations and plausible methods, such as soil application and foliar spray, of applications to stressed plants. Also, it will be great if microbial strains producing serotonin and melatonin in large amounts are identified and inoculated to plant vicinity as bioagent for stress management.

References Afreen, F., Zobayed, S., Kozai, T., 2006. Melatonin in Glycyrrhiza uralensis: response of plant roots to spectral quality of light and UV-B radiation. J. Pineal Res. 41, 108 115. Alvarez, A., Montesano, M., Schmelz, E., Ponce de Leo´n, I., 2016. Activation of shikimate, phenylpropanoid, oxylipins, and auxin pathways in Pectobacterium carotovorum elicitors-treated moss. Front. Plant Sci. 7, 328. Antoniou, C., Chatzimichail, G., Xenofontos, R., Pavlou, J.J., Panagiotou, E., Christou, A., et al., 2017. Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism. J. Pineal Res. 62, 1 14. Arnao, M.B., Herna´ndez-Ruiz, J., 2009. Chemical stress by different agents affects the melatonin content of barley roots. J. Pineal Res. 46, 295 299.

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References

787

Arnao, M.B., Herna´ndez-Ruiz, J., 2014. Melatonin: possible role as light-protector in plants. UV Radiation: Properties, Effects, and Applications. Physics Research & Technology Series. Nova Science Publishing, pp. 79 92. Awasthi, R., Bhandari, K., Nayyar, H., 2015. Temperature stress and redox homeostasis in agricultural crops. Front. Environ. Sci. 3, 1 24. Back, K., Tan, D.X., Reiter, R.J., 2016. Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J. Pineal Res. 61, 426 437. Balzer, I., Hardeland, R., 1996. Melatonin in algae and higher plants - possible new roles as a phytohormone and antioxidant. Bot. Acta 109, 180 183. Bita, C.E., Gerats, T., 2013. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front. Plant Sci. 4, 273. Available from: https://doi.org/10.3389/ fpls.2013.00273. Bornman, J.F., Barnes, P.W., Robinson, S.A., Ballare, C.L., Flint, S., Caldwell, M.M., 2015. Solar ultraviolet radiation and ozone depletion-driven climate change: effects on terrestrial ecosystems. Photochem. Photobiol. Sci. 14, 88 107. Bowden, K., Brown, B.G., Batty, J.E., 1954. 5-Hydroxytryptamine: its occurrence in cowhage. Nature 174, 925. Byeon, Y., Back, K., 2014. Melatonin synthesis in rice seedlings in vivo is enhanced at high temperatures and under dark conditions due to increased serotonin N-acetyltransferase and N-acetylserotonin methyltransferase activities. J. Pineal Res. 56, 189 195. Byeon, Y., Back, K., 2016. Low melatonin production by suppression of either serotonin N-acetyltransferase or Nacetylserotonin methyltransferase in rice causes seedling growth retardation with yield penalty, abiotic stress susceptibility, and enhanced coleoptile growth under anoxic conditions. J. Pineal Res. 60, 348 359. Byeon, Y., Lee, H.Y., Lee, K., Park, S., Back, K., 2014. Cellular localization and kinetics of the rice melatonin biosynthetic enzymes SNAT and ASMT. J. Pineal Res. 56, 107 114. Byeon, Y., Lee, H.Y., Hwang, O.J., Lee, H.J., Lee, K., Back, K., 2015a. Coordinated regulation of melatonin synthesis and degradation genes in rice leaves in response to cadmium treatment. J. Pineal Res. 58, 470 478. Byeon, Y., Tan, D.X., Reiter, R.J., Back, K., 2015b. Predominance of 2-hydroxymelatonin over melatonin in plants. J. Pineal Res. 59, 448 454. Cai, S.Y., Zhang, Y., Xu, Y.P., Qi, Z.Y., Li, M.Q., Ahammed, G.J., et al., 2017. HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants. J. Pineal Res. 62, 1 12. Chen, Z., Xie, Y., Gu, Q., Zhao, G., Zhang, Y., Cui, W., et al., 2017. The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic. Biol. Med. 108, 465 477. Cruz de Carvalho, M.H., 2008. Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal. Behav. 3, 156 165. Dawood, M.G., El-Awadi, M.E., 2015. Alleviation of salinity stress on Vicia faba L. plants via seed priming with melatonin. Acta Biolo´gica Colombiana 20, 223 235. De Luca, V., Marineau, C., Brisson, N., 1989. Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal dopa decarboxylases. Proc. Natl. Acad. Sci. U.S.A. 86, 2582 2586. Dharmawardhana, P., Ren, L., Amarasinghe, V., Monaco, M., Thomason, J., Ravenscroft, D., et al., 2013. A genome scale metabolic network for rice and accompanying analysis of tryptophan, auxin and serotonin biosynthesis regulation under biotic stress. Rice 6, 15. Dubbels, R., Reiter, R.J., Klenke, E., Goebel, A., Schnakenberg, E., Ehlers, C., et al., 1995. J. Pineal Res. 18, 28. Eapen, S., D’souza, S., 2005. Prospects of genetic engineering of plants for phytoremediation of toxic metals. Biotechnol. Adv. 23, 97 114. Erland, L.A.E., Saxena, P.K., 2017. Beyond a neurotransmitter: the role of serotonin in plants. Neurotransmitter 4, 1 12. Farooq, M., Gogoi, N., Hussain, M., Barthakur, S., Paul, S., Bharadwaj, N., et al., 2017. Effects, tolerance mechanisms and management of salt stress in grain legumes. Plant Physiol. Biochem. 118, 199 217. Fidalgo, F., Azenha, M., Silva, A.F., Sousa, A., Santiago, A., Ferraz, P., et al., 2013. Copper-induced stress in Solanum nigrum L. and antioxidant defense system responses. Food Energy Secur. 2, 70 80.

Plant Life under Changing Environment

788

31. Role of melatonin and serotonin in plant stress tolerance

Galano, A., Medina, M.E., Tan, D.X., Reiter, R.J., 2015. Melatonin and its metabolites as copper chelating agents and their role in inhibiting oxidative stress: a physicochemical analysis. J. Pineal Res. 58, 107 116. Gill, S.S., Hasanuzzaman, M., Nahar, K., Macovei, A., Tuteja, N., 2013. Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol. Biochem. 63, 254 261. Gu, Q., Chen, Z., Yu, X., Cui, W., Pan, J., Zhao, G., et al., 2017. Melatonin confers plant tolerance against cadmium stress via the decrease of cadmium accumulation and reestablishment of microRNA-mediated redox homeostasis. Plant Sci. 261, 28 37. Hardeland, R., 2016. Melatonin in plants diversity of levels and multiplicity of functions. Front. Plant Sci. 7, 198. Hasan, M., Ahammed, G.J., Yin, L., Shi, K., Xia, X., Zhou, Y., et al., 2015a. Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Front. Plant Sci. 6, 601. Hasan, M.K., Ahammed, G.J., Yin, L., Shi, K., Xia, X., Zhou, Y., et al., 2015b. Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Front. Plant Sci. 6, 601. Hatfield, J.L., Prueger, J.H., 2015. Temperature extremes: effect on plant growth and development. Weather Clim. Extremes 10, 4 10. Hemantaranjan, A., Bhanu, A.N., Singh, M., Yadav, D., Patel, P., Singh, R., et al., 2014. Heat stress responses and thermotolerance. Adv. Plants Agric. Res 1, 62 70. Hernandez, L., Garate, A., Carpena-Ruiz, R., 1997. Effects of cadmium on the uptake, distribution and assimilation of nitrate in Pisum sativum. Plant Soil 189, 97 106. Hossain, M., Hossain, M., Rohman, M., da Silva, J.T., Fujita, M., 2012a. Onion major compounds (flavonoids, organosulfurs) and highly expressed glutathione-related enzymes: possible physiological interaction, gene cloning and abiotic stress response. Onion Consumption and Health. Nova Science Publishers Inc, NY, pp. 49 90. Hossain, M.A., Piyatida, P., da Silva, J.A.T., Fujita, M., 2012b. Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J. Bot. 2012, 1 37. Ishihara, A., Hashimoto, Y., Miyagawa, H., Wakasa, K., 2008a. Induction of serotonin accumulation by feeding of rice striped stem borer in rice leaves. Plant Signal. Behav. 3, 714 716. Ishihara, A., Hashimoto, Y., Tanaka, C., Dubouzet, J.G., Nakao, T., Matsuda, F., et al., 2008b. The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production. Plant J. 54, 481 495. Janska´, A., Marsı´k, P., Zelenkova´, S., Ovesna´, J., 2010. Cold stress and acclimation what is important for metabolic adjustment? Plant Biol. 12, 395 405. Ja¨rup, L., 2003. Hazards of heavy metal contamination. Br. Med. Bull. 68, 167 182. Kang, S., Kang, K., Lee, K., Back, K., 2007. Characterization of rice tryptophan decarboxylases and their direct involvement in serotonin biosynthesis in transgenic rice. Planta 227, 263 272. Kang, K., Kang, S., Lee, K., Park, M., Back, K., 2008. Enzymatic features of serotonin biosynthetic enzymes and serotonin biosynthesis in plants. Plant Signal. Behav. 3, 389 390. Kang, K., Park, S., Kim, Y.S., Lee, S., Back, K., 2009. Biosynthesis and biotechnological production of serotonin derivatives. Appl. Microbiol. Biotechnol. 83, 27 34. Kar, R.K., 2011. Plant responses to water stress: role of reactive oxygen species. Plant Signal. Behav. 6, 1741 1745. Kavamura, V.N., Esposito, E., 2010. Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol. Adv. 28, 61 69. Kolar, J., Machackova, I., Eder, J., Prinsen, E., van Dongen, W., van Onckelen, H., et al., 1997. Melatonin: occurrence and daily rhythm in Chenopodium rubrum. Phytochemistry 44, 1407. Kopin, I.J., Pare, C., Axelrod, J., Weissbach, H., 1961. The fate of melatonin in animals. J. Biol. Chem. 236, 1961 3075. Kostopoulou, Z., Therios, I., Roumeliotis, E., Kanellis, A.K., Molassiotis, A., 2015. Melatonin combined with ascorbic acid provides salt adaptation in Citrus aurantium L. seedlings. Plant Physiol. Biochem. 86, 155 165. Kumar, J., Singh, S., Singh, M., Srivastava, P.K., Mishra, R.K., Singh, V.P., et al., 2017. Transcriptional regulation of salinity stress in plants: a short review. Plant Gene 11, 160 169. Larkindale, J., Vierling, E., 2008. Core genome responses involved in acclimation to high temperature. Plant Physiol. 146, 748 761.

Plant Life under Changing Environment

References

789

Lea, P.J., Miflin, B.J., 2003. Glutamate synthase and the synthesis of glutamate in plants. Plant Physiol. Biochem. 41, 555 564. Lee, K., Choi, G.H., Back, K., 2017. Cadmium-induced melatonin synthesis in rice requires light, hydrogen peroxide, and nitric oxide: key regulatory roles for tryptophan decarboxylase and caffeic acid O-methyltransferase. J. Pineal Res. 63, e12441. Lee Hyoung, Y., Byeon, Y., Tan, D.X., Reiter Russel, J., Back, K., 2015. Arabidopsis serotonin N-acetyltransferase knockout mutant plants exhibit decreased melatonin and salicylic acid levels resulting in susceptibility to an avirulent pathogen. J. Pineal Res. 58, 291 299. Lei, X.Y., Zhu, R.Y., Zhang, G.Y., Dai, Y.R., 2004. Attenuation of cold-induced apoptosis by exogenous melatonin in carrot suspension cells: the possible involvement of polyamines. J. Pineal Res. 36, 126 131. Lerner, A.B., Case, J.D., Takahashi, Y., Lee, T.H., Mori, W., 1958. Isolation of melatonin, the pineal gland factor that lightens melanocytes. J. Am. Soc. 80, 2587. Li, C., Wang, P., Wei, Z., Liang, D., Liu, C., Yin, L., et al., 2012. The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. J. Pineal Res. 53, 298 306. Li, C., Liang, B., Chang, C., Wei, Z., Zhou, S., Ma, F., 2016a. Exogenous melatonin improved potassium content in Malus under different stress conditions. J. Pineal Res. 61, 218 229. Li, M.Q., Hasan, Md, K., Li, C.X., Ahammed Golam, J., Xia, X.J., Shi, K., et al., 2016b. Melatonin mediates selenium-induced tolerance to cadmium stress in tomato plants. J. Pineal Res. 61, 291 302. Li, H., Chang, J., Chen, H., Wang, Z., Gu, X., Wei, C., et al., 2017. Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Front. Plant Sci. 8, 295. Liang, C., Zheng, G., Li, W., Wang, Y., Hu, B., Wang, H., et al., 2015. Melatonin delays leaf senescence and enhances salt stress tolerance in rice. J. Pineal Res. 59, 91 101. Ludwig-Mu¨ller, J., Cohen, J.D., 2002. Identification and quantification of three active auxins in different tissues of Tropaeolum majus. Physiol. Plant. 115, 320 329. Ma, X., Idle, J.R., Krausz, K.W., Gonzalez, F.J., 2005. Metabolism of melatonin by human cytochromes p450. Drug Metab. Dispos. 33, 489 494. Maestri, E., Klueva, N., Perrotta, C., Gulli, M., Nguyen, H.T., Marmiroli, N., 2002. Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol. Biol. 48, 667 681. Miransari, M., 2011. Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol. Adv. 29, 645 653. Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405 410. Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F., 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490 498. Mukherjee, S., David, A., Yadav, S., Baluˇska, F., Bhatla, S.C., 2014. Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiol. Plant. 152, 714 728. Murch, S.J., Saxena, P.K., 2002. Melatonin: a potential regulator of plant growth and development? In Vitro Cell. Dev. Biol. Plant 38, 531 536. Murch, S.J., KrishnaRaj, S., Saxena, P.K., 2000. Tryptophan is a precursor for melatonin and serotonin biosynthesis in in vitro regenerated St. John’s wort (Hypericum perforatum L. cv. Anthos) plants. Plant Cell Rep. 19, 698 704. Muscolo, A., Junker, A., Klukas, C., Weigelt-Fischer, K., Riewe, D., Altmann, T., 2015. Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions. J. Exp. Bot. 66, 5467 5480. Nicaise, V., Roux, M., Zipfel, C., 2009. Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol. 150, 1638 1647. Nishiuchi, S., Yamauchi, T., Takahashi, H., Kotula, L., Nakazono, M., 2012. Mechanisms for coping with submergence and waterlogging in rice. Rice 5, 2. Normanly, J., Bartelt, B., 1999. Redundancy as a way of life-IAA metabolism. Curr. Opin. Plant Biol. 2, 207 213. Osakabe, Y., Osakabe, K., Shinozaki, K., Tran, L.-S.P., 2014. Response of plants to water stress. Front. Plant Sci. 5, 86. Paredes, S.D., Barriga, C., Reiter, R.J., Rodrı´guez, A.B., 2009. Assessment of the potential role of tryptophan as the precursor of serotonin and melatonin for the aged sleep-wake cycle and immune function: Streptopelia Risoria as a model. Int. J. Tryptophan Res. 2, 23 36. Park, S., Back, K., 2012. Melatonin promotes seminal root elongation and root growth in transgenic rice after germination. J. Pineal Res. 53, 385 389.

Plant Life under Changing Environment

790

31. Role of melatonin and serotonin in plant stress tolerance

Ponce de Leo´n, I., Montesano, M., 2013. Activation of defense mechanisms against pathogens in mosses and flowering plants. Int. J. Mol. Sci. 14, 3178. Posmyk, M.M., Janas, K.M., 2008. Melatonin in plants. Acta Physiol. Plant. 31, 1. Qian, Y., Tan, D.-X., Reiter, R.J., Shi, H., 2015. Comparative metabolomic analysis highlights the involvement of sugars and glycerol in melatonin-mediated innate immunity against bacterial pathogen in Arabidopsis. Sci. Rep. 5, 15815. Rhodes, D., & Nadolska-Orczyk, A. (2001). Plant stress physiology. In eLS, (Ed.). Available from: https://doi. org/10.1038/npg.els.0001297. Sakamoto, A., Murata, N., 2002. The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 25, 163 171. Sharma, S.S., Dietz, K.-J., 2009. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 14, 43 50. Shi, H., Jiang, C., Ye, T., Tan, D.-X., Reiter, R.J., Zhang, H., et al., 2014. Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. J. Exp. Bot. 66, 681 694. Shi, H., Chen, Y., Tan, D.X., Reiter Russel, J., Chan, Z., He, C., 2015. Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis. J. Pineal Res. 59, 102 108. Singh, S., Parihar, P., Singh, R., Singh, V.P., Prasad, S.M., 2015. Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front. Plant Sci. 6, 1143. Steffens, D., Hutsch, B., Eschholz, T., Losak, T., Schubert, S., 2005. Water logging may inhibit plant growth primarily by nutrient deficiency rather than nutrient toxicity. Plant Soil Environ. 51, 545. Tan, D.-X., Manchester, L.C., Helton, P., Reiter, R.J., 2007a. Phytoremediative capacity of plants enriched with melatonin. Plant Signal. Behav. 2, 514 516. Tan, D.X., Manchester, L.C., Terron, M.P., Flores, L.J., Reiter, R.J., 2007b. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J. Pineal Res. 42, 28 42. Tan, D.X., Manchester, L.C., Liu, X., Rosales-Corral, S.A., Acuna-Castroviejo, D., Reiter, R.J., 2013. Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin’s primary function and evolution in eukaryotes. J. Pineal Res. 54, 127 138. Tanaka, E., Tanaka, C., Mori, N., Kuwahara, Y., Tsuda, M., 2003. Phenylpropanoid amides of serotonin accumulate in witches’ broom diseased bamboo. Phytochemistry 64, 965 969. Tang, Y., Lin, L., Xie, Y., Liu, J., Sun, G., Li, H., et al., 2018. Melatonin affects the growth and cadmium accumulation of Malachium aquaticum and Galinsoga parviflora. Int. J. Phytorem. 20, 295 300. Tettamanti, C., Cerabolini, B., Gerola, P., Conti, A., 2000. Melatonin identification in medicinal plants. Acta Phytotherapeutica 3, 137 144. Turk, H., Erdal, S., Genisel, M., Atici, O., Demir, Y., Yanmis, D., 2014. The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul. 74, 139 152. Verdaguer, D., Jansen, M.A.K., Llorens, L., Morales, L.O., Neugart, S., 2017. UV-A radiation effects on higher plants: exploring the known unknown. Plant Sci. 255, 72 81. Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R., 2007. Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199 223. Wang, P., Yin, L., Liang, D., Li, C., Ma, F., Yue, Z., 2012. Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate glutathione cycle. J. Pineal Res. 53, 11 20. Wang, P., Sun, X., Li, C., Wei, Z., Liang, D., Ma, F., 2013. Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. J. Pineal Res. 54, 292 302. Wang, L., Feng, C., Zheng, X., Guo, Y., Zhou, F., Shan, D., et al., 2017. Plant mitochondria synthesize melatonin and enhance the tolerance of plants to drought stress. J. Pineal Res. 63, e12429. Xu, W., Cai, S.Y., Zhang, Y., Wang, Y., Ahammed, G.J., Xia, X.J., et al., 2016. Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. J. Pineal Res. 61, 457 469. Yin, L., Wang, P., Li, M., Ke, X., Li, C., Liang, D., et al., 2013. Exogenous melatonin improves Malus resistance to Marssonina apple blotch. J. Pineal Res. 54, 426 434.

Plant Life under Changing Environment

References

791

Zhang, L., Jia, J., Xu, Y., Wang, Y., Hao, J., Li, T., 2012. Production of transgenic Nicotiana sylvestris plants expressing melatonin synthetase genes and their effect on UV-B-induced DNA damage. In Vitro Cell. Dev. Biol.— Plant 48, 275 282. Zhang, H.J., Zhang, N., Yang, R.C., Wang, L., Sun, Q.Q., Li, D.B., et al., 2014a. Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J. Pineal Res. 57, 269 279. Zhang, N., Sun, Q., Zhang, H., Cao, Y., Weeda, S., Ren, S., et al., 2014b. Roles of melatonin in abiotic stress resistance in plants. J. Exp. Bot. 66, 647 656. Zhang, S., Zheng, X., Reiter, R.J., Feng, S., Wang, Y., Liu, S., et al., 2017. Melatonin attenuates potato late blight by disrupting cell growth, stress tolerance, fungicide susceptibility and homeostasis of gene expression in Phytophthora infestans. Front. Plant Sci. 8, 1 19. Zheng, X., Zhou, J., Tan, D.-X., Wang, N., Wang, L., Shan, D., et al., 2017. Melatonin improves waterlogging tolerance of Malus baccata (Linn.) Borkh. seedlings by maintaining aerobic respiration, photosynthesis and ROS migration. Front. Plant Sci. 8, 483. Zhu, J.-K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247 273. Zipfel, C., 2009. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12, 414 420. Zou, J., Liu, A., Chen, X., Zhou, X., Gao, G., Wang, W., et al., 2009. Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J. Plant Physiol. 166, 851 861. Zuo, B., Zheng, X., He, P., Wang, L., Lei, Q., Feng, C., et al., 2014. Overexpression of MzASMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis thaliana plants. J. Pineal Res. 57, 408 417.

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32 Role of nitric oxide dependent posttranslational modifications of proteins under abiotic stress Mounira Chaki, Juan C. Begara-Morales, Raquel Valderrama, Capilla Mata-Pe´rez, Marı´a N. Padilla-Serrano and Juan B. Barroso Group of Biochemistry and Cell Signalling in Nitric Oxide, Department of Experimental Biology, Faculty of Experimental Sciences, Center for Advanced Studies in Olive Grove and Olive Oils, University of Jae´n, Campus Universitario “Las Lagunillas” s/n, Jae´n, Spain

32.1 Introduction Plant growth and development are influenced by continuous changing environments, these adverse conditions include abiotic stress such as heat, cold, wounding, drought, light intensity, ozone, nutrient deficiency, toxic metals such as cadmium, arsenate, and aluminum, and excessive salts affecting plant development and reproduction (Mittler, 2006). Many of these stress conditions could extremely change the response of plant cells to this potential damage causing a wide influence on crop productivity and consequently great economic losses (Boyer, 1982). Environmental factors produce an abnormal generation of reactive oxygen species (ROS) such as hydrogen peroxide (H2O2), superoxide radicals (O2 2 ), and hydroxyl radicals (OH2) which can trigger an oxidative impairment to proteins, membrane lipids, and nucleic acids (Apel and Hirt, 2004). Moreover, cellular damage generated by abiotic stress can also be mediated by arise in nitric oxide (NO) and other molecules designed as reactive nitrogen species (RNS) inducing a nitrosative stress (Radi, 2004, 2012). When abiotic stress take place, an increase of ROS and RNS contents could mediate the impairment of important biomolecules, 2 for example, the interaction between O2 2 and NO generate peroxynitrite (ONOO ); a powerful oxidative agent that can react with carbon dioxide (CO2) and be further decomposed into CO2 3 and NO2 (Radi, 2013). To adapt to these stress conditions, plant cells modulate the redox homeostasis which is effected in part by the regulation of intracellular reactive oxygen and Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00035-7

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nitrogen species, particularly H2O2 and NO, that have been considered as the mean signaling molecules involved in the regulation of abiotic stress response in plant systems. NO is a free radical biological messenger, acts as a key signaling molecule in plant biology, and has an important role in response to physiological and abiotic stress processes (BessonBard et al., 2008; Qiao and Fan, 2008). It has been shown that NO regulates numerous development processes in higher plants including stomatal closure (Neill et al., 2002), flowering (He et al., 2004), seed germination (Bethke et al., 2004; Albertos et al., 2015), and senescence (Guo and Crawford, 2005; Du et al., 2014) as well as plays a well-established role in stressrelated processes (Barroso et al., 1999; Durner et al., 1998; Chaki et al., 2009a; Corpas et al., 2011; Fancy et al., 2016). There is a great interest for the involvement of NO and other RNS as signaling molecules in response to different abiotic stress situations. In this way, NO and NO-derived molecules can alter target proteins mainly via NO-related posttranslational modifications (PTMs) including S-nitrosylation, protein tyrosine nitration (NO2-Tyr), and nitroalkylation (Fig. 32.1), which can regulate protein function (Corpas et al., 2015;

FIGURE 32.1 Schematic model of NO-dependent posttranslational modifications in plant cells. NO can be produced by L-arginine-dependent nitric oxide syntase (NOS), nitro-fatty acids (NO2-FA), nitrate reductase (NR), or other nonenzymatic source. Dinitrogen dioxide (N2O3) generated by NO can react with reduced glutathione (GSH) to form S-nitrosoglutathione (GSNO) (1) which could mediate protein S-nitrosylation under abiotic stress conditions, contributing in a signaling actions (2). Furthermore, NO can react with superoxide radicals (O22) to generate peroxynitrite (ONOO2) that can mediate protein tyrosine nitration under abiotic stress leading to a nitrosative stress (3). Moreover, ONOO2 can generate nitrogen dioxide ( NO2) which can mediate NO2-FA formation under environmental stress conditions (4). The electrophilic ability of nitro-fatty acid could mediate nitroalkylation reactions with cysteine, histidine, or lysine residues contributing to the signaling processes (5).




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Geisler and Rudolph, 2012). Increasing studies suggest that these NO-dependent PTMs could be important in maintaining the redox homeostasis by the regulation of the antioxidant systems. Although a high number of proteins have been reported as targets of these redox PTMs under physiological and abiotic stress, the knowledge of the impact on particular proteins is unknown in the most of cases. In this chapter, we will provide recent information regarding the impact of NO-PTMs on protein function and its outcome on plant response to adverse environmental factors.

32.2 Nitric oxide dependent posttranslational modification of proteins under abiotic stress 32.2.1 Protein S-nitrosylation under adverse environmental stress conditions S-Nitrosothiols (SNOs) stem from the reaction of NO with thiol groups of cysteine (Cys) residues of proteins. These molecules are highly weak in an intracellular redox medium; for this they are sensitive mechanisms in the regulation of cellular processes. S-Nitrosoglutathione (GSNO) is a low-molecular-weight SNO that is produced by the S-nitrosylation reaction of NO with glutathione. GSNO is considered important in the regulation of NO-dependent events. It has been used to generate S-nitrosylated target proteins in plant extracts (Lindermayr et al., 2005; Chaki et al., 2015). Protein S-nitrosylation is a redox-based PTM mechanism which consists to the covalent binding of NO to the sulfhydryl group of a protein Cys thiol, leading to the SNOs formation (Jaffrey and Snyder, 2001; Stamler et al., 2001). It can also be achieved through the exchange of NO molecule from an S-nitrosylated protein in a so-called trans-nitrosylation reaction (Lindermayr and Durner, 2009; Wang et al., 2006). This NO-dependent PTM is the main redox signaling mechanism by which NO transmits its bioactivity. It has been shown that the S-nitrosylation regulates protein functions by several mechanisms, such as cellular localization, enzymatic activity, protein protein interaction, and three-dimensional conformation changes (Benhar and Stamler, 2005; Hess et al., 2005; Astier et al., 2011; Gupta, 2011). The binding and elimination of NO to the protein is not exactly an enzymatic process; however, it depends principally on the cellular redox status (Lindermayr and Durner, 2009) and is considered as one of the functionally interesting forms of physiological NO-PTM in plant systems. Until now, the basis to resolve the NO target residues is not clear. It has proposed that the presence of acid base motif next to the Cys residues is necessary (Stamler et al., 2001). However, other studies have suggested that the three-dimensional environment establishes the sensitive residues to S-nitrosylation (Taldone et al., 2005). Identification of potential target proteins for S-nitrosylation and their modified residue(s) is vital to study the regulatory functions of this modification in higher plants. The biotin switch technique (BST) (Jaffrey and Snyder, 2001) is a principal approach which allowed the detection of potential target proteins for S-nitrosylation under physiological and adverse environmental insults in plant systems (Lindermayr et al., 2005; Hu et al., 2015). BST is based on several steps; blocking of free Cys residues by methanethiol sulfonate, breaking of NO-Cys bonds by a reducing agent such as ascorbate following the attachment of biotin to Cys residues. This assay allows the identification of S-nitrosylated proteins by antibiotin antibody or their isolation by neutravidin matrix. Afterward, the Plant Life under Changing Environment

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identified candidates could be detected by mass spectrometry. Although the method is relatively simple, due to different technical limitations, the number of the identified targets is limited (Torta et al., 2008). Therefore the computational methods are attracting a wide interest for the identification of S-nitrosylated proteins (Xue et al., 2010; Lee et al., 2011; Xu et al., 2013a,b). A recently developed GPS-SNO 1.0 software (Xue et al., 2010) was used for the prediction of the NO-sensitive Cys residue(s) for S-nitrosylation in Arabidopsis plants. A total of 16,610 target proteins for S-nitrosylation with 31,900 Snitrosylated sites were isolated from Arabidopsis proteome, and the predicted candidates involved in the signaling processes exhibited the highest prediction rate (Chaki et al., 2014). The authors proposed that these methods were good tools, nevertheless, additional development of the software is needed, such as including the three-dimensional structure of proteins might increase the identification of modified residues. Protein S-nitrosylation has been emerged as one of the most important NO-PTM which regulates important processes in plant biology including plant immunity or plant response to different biotic and abiotic stress situations (Romero-Puertas et al., 2008; Fares et al., 2011). Therefore this modification has become the principal way by which NO acts as a signal molecule. In this respect the number of S-nitrosylated proteins identified by proteomic methods was increased. However, the specific impact is unknown in most of the identified candidates (Lin et al., 2012; Tanou et al., 2012). The pioneer study of protein S-nitrosylation in plant systems was realized by Lindermayr et al. (2005). In this study, 52 proteins from NO-treated leaves and 63 proteins from Arabidopsis cell culture extracts treated by GSNO were detected as potential targets for S-nitrosylation, that are implicated in cellular signaling, stress response, metabolic processes, redox homeostasis, and cytoskeleton organization (Lindermayr et al., 2005). Afterward, applied studies confirmed and extended the number of identified targets under physiological and different stress conditions (reviewed by Mata-Pe´rez et al., 2016a,b). Nitrosoproteome in plants was also identified by site-specific strategy. In this approach the biotinylated proteins were digested and the enriched peptides were identified by mass spectrometry (Hao et al., 2006; Chen et al., 2010; Hu et al., 2015). Using this approach, Hu et al. (2015) have been identified 1195 endogenously S-nitrosylated peptides from Arabidopsis that is the major data set of S-nitrosylated proteins identified until now (Hu et al., 2015). Modulation of SNO levels as well as ROS and RNS has been reported in several plant species exposed to adverse environmental factors (Corpas et al., 2011; Fancy et al., 2016). The majority of the S-nitrosylated candidate proteins implicated in the response to environmental stresses are redox-related proteins including antioxidant proteins or ROS generating enzymes proposing a function of S-nitrosylation as an important regulator of the redox homeostasis during the abiotic stress situations. Also, it has been suggested that this NO-PTM could be implicated in the protection against oxidative stress (Tanou et al., 2009; Begara-Morales et al., 2014b). Until now, there is limited information regarding the role of S-nitrosylation as a regulator of redox signaling pathways in response to environmental insults. 32.2.1.1 Extreme temperatures Extreme temperatures are the environmental factors with a high influence on plant growth and production. Extreme temperatures are expected to occur more often and more severely and affect plant growth and development in several ways, affecting the

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production component of food security. In general, heat stress produces heat shock protein families (Wang et al., 2004; Larkindale and Vierling, 2007) as well as an increase of ROS and RNS contents (Volkov et al., 2006; Suzuki and Mittler, 2006; Corpas et al., 2008; Chaki et al., 2011a; Ziogas et al., 2013). It has been shown that the defective mutants HOT5/ GSNOR1 revealed high levels of nitrate and nitroso species inducing heat sensitivity (Lee et al., 2008). Moreover, in sunflower plants subjected to high temperature, it found that the total SNOs and GSNO have been upregulated. Confocal laser scanning microscopy show GSNO localization in vascular tissue and epidermal cells; however, after heat stress higher levels were observed in epidermal cells proposing that the rise of GSNO in epidermis could be acting as a defense mechanism against external environment (Chaki et al., 2011a). On the other hand, cold stress has a negative effect on plant growth affecting photosynthesis and uptaking of nutrients and water. It has been reported that the cold stress regulates gene expression (Shinozaki et al., 2003) and was implicated in the metabolism of RNS (Corpas et al., 2008; Chaki et al., 2011b; Airaki et al., 2012; Sehrawat et al., 2013). In this sense, 15 target proteins for S-nitrosylation were identified in Brassica juncea exposed to low-temperature stress (4 C for 6 hours) including pathogenesis, metabolic (glycolysis), photosynthetic, and signaling proteins. RuBisCO was the major protein modulated by this stress; both up- and downregulations of RuBisCO nitrosylation by low temperature were observed (Abat and Deswal, 2009). Subsequently, Sehrawat et al. (2013) identified S-nitrosylated target proteins in RuBisCO depleted fractions, 78 spots detected as target proteins in response to cold stress (4 C for 6 hours), out of which 15 spots showed differential S-nitrosylation (Sehrawat et al., 2013). Likewise, in Arabidopsis plantlets 62 endogenously S-nitrosylated proteins were found, 20 of them over-nitrosylated following exposure to cold stress (4 C for 4 hours), suggesting that S-nitrosylation level could be differentially modulated under cold stress (Puyaubert et al., 2014). 32.2.1.2 Wounding Plants are constantly exposed to external stress situations including herbivores, insects, or abiotic sources that cause injuring, and open the way to the penetration of microbial pathogens. Affected tissues rapidly accumulate defensive secondary metabolites for fighting off microbial invaders or herbivorous attackers. Next, the wound zone is sealed by callose formation and induction of localized cell death. Plant injury provokes long-distance cascade of signals which could show some changes in ethylene, abscisic acid, and jasmonic acid among others (Leo´n et al., 2001; Stratmann, 2003). Likewise, the wound could also cause an increase of ROS that triggers the oxidative damage (Fernando Reyes et al., 2006; Miller et al., 2009; Chaki et al., 2011b). The total content of SNOs was increased in sunflower hypocotyls and in pea leaves subjected to wounding stress (Corpas et al., 2008; Chaki et al., 2011b). In addition, in extra fascicular phloem samples, SNO levels and protein S-nitrosylation were reduced after 6 48 hours of leaves wounding. Seven bands of approximately 16, 18, 29, 37, 50, 75, and 80 kDa were observed by western blot in extra fascicular phloem samples of control pumpkin but was weakened at 3 and 24 hours after wounding (Gaupels et al., 2016). The authors proposed that the observed wounding stress responses could be part of the extra fascicular phloem defense mechanisms produced by systemic messengers (Gaupels et al., 2016).

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32.2.1.3 Salinity Salt stress is another abiotic stress, which produce enormous losses in agricultural production, affect plant productivity due to alterations produced in respiration and photosynthesis, as well as in the metabolism of nucleic acids and proteins (Hasegawa et al., 2000). High salt concentrations can have a harmful outcome on plant metabolism, interrupting cellular homeostasis, and disconnecting key physiological processes. A direct consequence of salt stress, an increased accumulation of ROS, and ultimately an oxidative stress (Hasegawa et al., 2000; Chaves et al., 2009). Salt stress is also accompanied by the accumulation of NO and NO2-Tyr, that is considered a biomarker of nitrosative stress (Valderrama et al., 2007). Plants develop several protective mechanisms against salt stress such as osmolyte biosynthesis, water transport, and ROS scavenging (Hasegawa et al., 2000). In olive plants grown under 200 mM NaCl, leaf fresh weight was reduced and accompanied with a disequilibrium between ROS production and antioxidant systems that induces an oxidative stress in plant cells (Valderrama et al., 2006), and a rise in total SNOs (Valderrama et al., 2007). The increase of total SNOs was also detected in pea plants exposed to salt stress (Begara-Morales et al., 2015). In citrus plants under salt stress, 49 target proteins for S-nitrosylation were reported (Tanou et al., 2009). Fares et al. (2011) combined BST and isotope-coded affinity tags labeling for the identification of endogenous S-nitrosylated proteins in Arabidopsis cell suspension subjected during 5 minutes to salt stress(100 mM NaCl) (Fares et al., 2011). Furthermore, the S-nitrosylation of APX and MDHAR have been shown in pea plants under 4 days salt stress (150 mM NaCl) (Begara-Morales et al., 2014a, 2015). S-Nitrosylation of APX at Cys 32 increased its activity; however, the S-nitrosylation of MDHAR at Cys 20 reduced it, suggesting that this difference in the activity might be due to a different S-nitrosylated target Cys (Begara-Morales et al., 2014a, 2015). Furthermore, the recombinant pea mitochondrial PsPrxII F was S-nitrosylated under salt stress reducing protein activity (Camejo et al., 2015). In addition the pattern of protein S-nitrosylation was studied in mitochondria of pea under salt stress (150 mM NaCl) during 5 and 14 days. Less number of target proteins have been observed at 14 days, including respiratory and photorespiratory-related enzymes, suggesting that the low S-nitrosylation observed at 14 days could allowed proteins related to respiration and photorespiration to be functional in conditions where these processes have an important role in establishing the tolerance to this environmental stress (Camejo et al., 2013). 32.2.1.4 Heavy metals Environmental contamination by heavy metals is increasing in the world and represents a growing threat to humans, animals, and plants. Plant species have a basal tolerance to heavy metals; however, higher concentrations may become toxic and cause dangerous effects and disturbances including transpiration and photosynthesis inhibition, nutrition stress, disturbance of carbohydrate metabolism and oxidative stress, all of which affect plant development and growth (Kra¨mer and Clemens, 2005). Plants respond to heavy metals by production of phytochelatins, that bind toxic metals (Pal and Rai, 2010; Gupta et al., 2013). The response of RNS to cadmium stress was described in pea leaves (Barroso et al., 2006). In Arabidopsis cells treated with cadmium, it was found that NO regulates the phytochelatin levels by S-nitrosylation (De Michele et al., 2009).

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Nevertheless, the S-nitrosylation levels of pea peroxisomal proteins glycolate oxidase and catalase changed under cadmium stress, suggesting that this NO-dependent PTM could be implicated in the regulation of H2O2 content during this abiotic stress (Ortega-Galisteo et al., 2012). 32.2.1.5 Ozone Ozone exerts dual functional effects on earth; depending on its localization, the stratospheric ozone protects from unsafe ultraviolet radiation; however, the tropospheric ozone produces an oxidative stress and ultimately causes cell death (Langebartels et al., 2002; Kangasja¨rvi et al., 2005) producing significant agricultural crop loss (Fares et al., 2013). Temporary exposure to high-level of ozone induces changes in protein activity and gene expression (Vainonen and Kangasja¨rvi, 2015). With this respect, in poplar leaves fumigated by ozone, 32 proteins detected as targets for S-nitrosylation, the content of S-nitrosylated candidates increased in 9 and decreased in 23 proteins; some of them are antioxidant candidates and therefore involved in redox homeostasis (Vanzo et al., 2014). In gray poplar the S-nitrosylated target proteins increased under a strong ozone stress; however, the changes in the nitrosoproteome of the nonisoprene-emitting genotype were much more observed than in the isoprene-emitting genotype (Vanzo et al., 2016). The authors proposed that isoprene regulates the production of ROS by the control of S-nitrosylated ROS-metabolizing proteins.

32.2.2 Protein tyrosine nitration during abiotic stress situations Protein tyrosine nitration is an oxidative PTM which is mediated by NO-derived molecules. In animals, NO2-Tyr is being used as a nitro-oxidative stress biomarker (Schopfer et al., 2003) rather than a modification involved in signaling processes. NO2-Tyr can alter the protein structure, the catalytic activity, and the protein susceptibility to proteolysis. The affected proteins lost the function, while, in some cases, the protein has also been described gain-of-function. Plants exposed to adverse environmental factors are usually accompanied by a nitro-oxidative stress (Begara-Morales et al., 2014a), with a simultaneous increase in NO2-Tyr which could be considered a footprint of nitro-oxidative stress (Corpas et al., 2007). In higher plants a significant number of results support this data since an increase of specific NO2-Tyr under stress conditions has been described (reviewed by Mata-Pe´rez et al., 2016a). At present, most investigations on NO2-Tyr in plant systems have carried out under adverse environmental stress situations. Nonetheless, most of these studies have indicated that protein tyrosine nitration also happens at the physiological levels (Chaki et al., 2009b). Two principal methods have been used for the identification of nitrated proteins in plant systems. The first one is based on the use of an antibody against 3-nitrotyrosine, which allowed the identification of immunoreactive bands (Valderrama et al., 2007; Chaki et al., 2009a; Wisastra et al., 2011). The second method is carried out by mainly using two-dimensional polyacrylamide gel electrophoresis and mass spectrometry identification of immunoreactive spots (Chaki et al., 2009b). The proteomic analyses used for the identification of the target proteins have shown that the identity and the number of the

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identified candidate proteins change amongst organs studied, plant species, and growing situations. The available studies in plant systems have increased significantly under adverse environmental stress conditions and have accepted that an increase in NO2-Tyr is a good marker of nitro-oxidative stress (Corpas and Barroso, 2013), study which can give an extensive overview of the importance of this NO-PTM in plant physiology. However, there are a few target proteins in which nitrated tyrosine residues have been identified. The characterization of the identified candidates is crucial to confirm the protein targets identified by the proteomic approaches and to analyze the impact of this NO-PTM in plant cells under environmental stress situation. Most analyses of NO2-Tyr in plant systems have shown that usually the nitrated proteins lost the function (Corpas et al., 2013b). The loss of protein activity was observed in tobacco APX (Clark et al., 2000), sunflower S-adenosylhomocysteine hydrolase, ferredoxin NADP reductase and carbonic anhydrase (Chaki et al., 2009b, 2011a, 2013), Arabidopsis O-acetylserine(thiol)lyase A1 (Alvarez et al., 2011), and NADH-dependent HPR1 (Corpas et al., 2013a). Mass spectrometry analysis of NADH-dependent HPR1 showed Tyr-97, Tyr-108, and Tyr-198 as nitrated targets. Using site-directed mutagenesis, Tyr-198 is identified as the nitrated residue responsible for the reduction of protein activity (Corpas et al., 2013a). The activity was also reduced in pea NADP-ICDH (Begara-Morales et al., 2013) and cytosolic APX (Begara-Morales et al., 2014a), and mass spectrometric analysis of cytosolic APX allowed the identification of Tyr-5 and Tyr-235 as nitrated targets (Begara-Morales et al., 2014a). 32.2.2.1 Extreme temperatures The NO2-Tyr levels have been identified in pea seedlings exposed to low and high temperature; a clear intensification of immunoreactive bands was observed with both stress situations (Corpas et al., 2008). In addition the metabolism of RNS was analyzed in sunflower seedlings subjected to high temperature (38 C for 4 hours). The authors have shown that the rise in total SNO levels was responsible for the increase of NO2-Tyr and ONOO2 contents under heat stress inducing a nitrosative stress (Chaki et al., 2011a). The nitroproteome analysis allowed the identification of 13 target proteins for nitration after heat stress involving in different functional categories including antioxidant, metabolism, photosynthesis, and carbohydrate, among others (Chaki et al., 2011a). Amongst the induced candidates, ferredoxin NADP reductase and carbonic anhydrase are the main proteins involved in photosynthetic carbon assimilation, a process very sensitive to high temperature (Chaki et al., 2011a, 2013). Activity of these proteins was inhibited by ONOO2 as nitrating agent suggesting that heat stress augments SNOs, which appear to mediate NO2-Tyr levels (Chaki et al., 2011a, 2013). In pepper plants subjected to cold stress (8 C) from 1 to 3 days an increase in NO2-Tyr after 24 hours of exposition was observed inducing a nitrosative stress (Airaki et al., 2012). Nonetheless, the continent of NO2-Tyr was decreased after the second and third day of treatment, which indicate that the acclimation of pepper plants to low temperature inverted the nitrosative stress observed at 24 hours (Airaki et al., 2012).

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32.2.2.2 Wounding In sunflower hypocotyls the NO2-Tyr levels were increased after mechanical wounding (4 hours). Using confocal laser scanning microscopy, the content of NO2-Tyr in unstressed sunflower hypocotyls showed an overall distribution in vascular tissues and cortex cells of nonstress plants. Nevertheless, after mechanical wounding, an increase of fluorescence was observed in all cell types (Chaki et al., 2011b). Chaki et al. (2011b) suggested that the SNOs could mediate the process of NO2-Tyr by a mechanism that involves the decomposition of SNOs and the formation of ONOO2 and, therefore, mediate the increase in NO2Tyr, suggesting that SNOs could be a wound signaling in sunflower plants. In addition, in pumpkin plants, NO2-Tyr increased after leaf injury, using antinitrotyrosine antibody 6 candidate tyrosine-nitrated phloem proteins, have been identified (Gaupels et al., 2016). 32.2.2.3 Salinity The metabolism of RNS was also studied in olive, Arabidopsis and citrus plants exposed to salt stress. In olive leaves grown under salinity stress (200 mM) a rise of the number and intensity of nitrated proteins and a general intensification of the NO2-Tyr in all cells were observed, an increase of RNS chiefly in the vascular tissue have also found (Valderrama et al., 2007). The authors suggest that salt stress produces a nitrosative stress in olive leaves, and vascular tissues could be involved in the redistribution of RNS (Valderrama et al., 2007). Furthermore, in Arabidopsis seedlings exposed to 100 mM NaCl, a rise in NO and ONOO2 contents was detected and is in correlation with the increase of NO2-Tyr (Corpas et al., 2009). Furthermore, the target proteins for nitration were identified in citrus trees exposed to 150 mM NaCl stress for 8 days; 88 target proteins were identified in leaves and 86 in roots (Tanou et al., 2012). Also, in sunflower seedlings (2-day-old) treated with 120 mM NaCl, an augmentation in protein tyrosine nitration was observed in the cells of columella and the peripheral cells (David et al., 2015). 32.2.2.4 Heavy metals Heavy metals can damage plant cells altering main plant physiological and metabolic processes. Analysis of NO2-Tyr content in leaves and roots of Arabidopsis seedlings subjected to arsenic stress showed that the nitrated proteins were in the range of 45 90 kDa with a significant change in some immune reactive bands (Leterrier et al., 2012). In the leaves, it was observed an intensification of the band of 60 kDa and its reduction in roots, suggesting that the difference of response in both organs to arsenic stress must be different (Leterrier et al., 2012). Moreover, a rise of ONOO2 content was reported in peroxisomes and cytosol of Arabidopsis plants exposed to cadmium stress (Corpas and Barroso, 2014). The authors proposed that peroxisomes could be a source of ONOO2, and the metabolism of NO-derived molecules in peroxisomes could be involved in the response to cadmium. Furthermore, the sensitivity of Brassica species (B. juncea and B. napus) to zinc stress has been studied. In fact, B. napus stored more zinc in its organs. In this sense the tolerance of B. napus shoot to zinc stress was accompanied by some changes in NO2-Tyr levels. However, the root of B. napus showed slighter increases in nitration pattern compared to B. juncea (Feigl et al., 2016).

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32.2.3 Nitrated fatty acids NO and others RNS can interact with a wide spectrum of biomolecules which affect their functions. During the last decade, there search on the interaction of RNS with other biomolecules has increased in animal systems. Nitro-fatty acids (NO2-FAs) result from the reaction of NO and other RNS with unsaturated FAs (Baker et al., 2009; Rudolph et al., 2010). This interaction produces a family of molecules with a longer half-life than NOrelated molecules. Several mechanisms of NO2-FAs formation have been proposed including nitrogen dioxide (NO2), nitrite (NO22), and ONOO2, nevertheless, until now the mechanism of in vivo nitration of FA is unknown (Freeman et al., 2008; Rubbo, 2013). NO2-FAs are proposed as new mediators in cell signaling. In animal systems, these signaling molecules are extensively studied; however, in plant organisms, they are scarcely explored. In extra virgin olive oil, the presence of free NO2-FAs and adducted proteins has been shown, suggesting that part of the cardiovascular benefits could be mediated by these nitrated lipid derivatives (Fazzari et al., 2014). Recently, the presence of nitrolinolenic acid (NO2-Ln) in Arabidopsis plants was reported, and its levels were analyzed under different abiotic stress conditions. In Arabidopsis cell cultures exposed to salt stress (100 mM NaCl) the NO2-Ln levels were upregulated after 5 minutes and downregulated after 30 minutes of treatment. Furthermore, in Arabidopsis seedlings (14-days-old) exposed to low-temperature, wounding, and cadmium stress, the NO2-Ln content increased, indicating the involvement of this NO2-FA in the response to several environmental insults (Mata-Pe´rez et al., 2016b). In addition, RNA-seq analyses have demonstrated its signaling role in plant defense against adverse environmental stress conditions inducing principally the chaperone network (Mata-Pe´rez et al., 2016b). On the other hand, Padilla et al. (2017) reported the role of NO2-Ln as a NO donor both in vitro and in vivo (Padilla et al., 2017). 32.2.3.1 Protein nitroalkylation Nitrated FAs act predominately via PTM. Due to its structure, the β-carbon adjacent to the carbon, attached to the nitro group (α-carbon), has a character of weak electrophile. Therefore the β-carbon is an exceptional target for nucleophilic attack. This reaction is known as Michael addition and involves the formation of a covalent bond between the nucleophile and electrophile and occurs mainly with Cys, His, and Lys residues on transcription regulating proteins (Schopfer et al., 2011; Geisler and Rudolph, 2012). NO2-FAs modify covalently different molecules affecting their structure and function (Batthyany et al., 2006); this reaction is recognized as nitroalkylation (Geisler and Rudolph, 2012). In animal organisms, there search to understand the interaction between NO and other RNS with NO2-FAs has been reached. In this regards, nitroalkylation of antioxidant and antiinflammatory proteins triggers the change of their activities, which provide interesting beneficial mechanisms (Schopfer et al., 2011; Villacorta et al., 2016). However, in higher plants to my knowledge, there is no information regarding this NO-dependent PTM; therefore analysis of the electrophilic ability of NO2-FA in plant exposed to different stress conditions could be helpful to understand the role of this NO2-FAs in higher plants under environmental factors.

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References

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32.3 Conclusions and perspectives This work provides a summary of the identified NO-sensitive target proteins in higher plants under adverse environmental stresses. The identification of candidate proteins putative NO targets using proteomics approaches increased in recent years. Nevertheless, only a limited number of the identified targets where the exact NO-sensitive sites have reported. In this regard, redox-biochemical analyses of the identified target proteins is a future challenge to know the mechanisms and the regulatory functions of these NOdependent PTMs on protein function and its impact on plant response to adverse environmental stress conditions. On the other hand the NO2-FAs presence and biological actions have extensively studied in animals, however, in higher plants these molecules have recently started to be investigated, with the endogenous detection of NO2-Ln in Arabidopsis plants. Thus it is very important to focus the future research on the identification and functional characterization of cellular target proteins of nitroalkylation mediated by nitrated FAs and their involvement in plant signaling mechanisms under physiological and stress situations. Indeed, NO2-FAs could be considered a promising new research area in NO field, which need to be carried out in plant organisms. In summary, further research will be required to study the impact of these NO-dependent PTMs in responses to adverse stress situations in different plant species in order to find biotechnological approaches to improve plant growth and crop yield under adverse environmental stress conditions.

References Abat, J.K., Deswal, R., 2009. Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9, 4368 4380. Available from: https://doi.org/10.1002/pmic.200800985. Airaki, M., Leterrier, M., Mateos, R.M., Valderrama, R., Chaki, M., Barroso, J.B., et al., 2012. Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ. 35, 281 295. Available from: https://doi.org/10.1111/j.1365-3040.2011.02310.x. Albertos, P., Romero-Puertas, M.C., Tatematsu, K., Mateos, I., Sa´nchez-Vicente, I., Nambara, E., et al., 2015. S-Nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat. Commun. 6. Available from: https://doi.org/10.1038/ncomms9669. Alvarez, C., Lozano-Juste, J., Romero, L.C., Garcı´a, I., Gotor, C., Leo´n, J., 2011. Inhibition of Arabidopsis O-acetylserine(thiol)lyase A1 by tyrosine nitration. J. Biol. Chem. 286, 578 586. Available from: https://doi. org/10.1074/jbc.M110.147678. Apel, K., Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant. Biol. 55, 373 399. Available from: https://doi.org/10.1146/annurev.arplant.55.031903.141701. Astier, J., Rasul, S., Koen, E., Manzoor, H., Besson-Bard, A., Lamotte, O., et al., 2011. S-Nitrosylation: an emerging post-translational protein modification in plants. Plant Sci. Available from: https://doi.org/10.1016/ j.plantsci.2011.02.011. Baker, P.R.S., Schopfer, F.J., O’Donnell, V.B., Freeman, B.A., 2009. Convergence of nitric oxide and lipid signaling: anti-inflammatory nitro-fatty acids. Free Radic. Biol. Med. Available from: https://doi.org/10.1016/ j.freeradbiomed.2008.11.021. Barroso, J.B., Corpas, F.J., Carreras, A., Sandalio, L.M., Valderrama, R., Palma, J.M., et al., 1999. Localization of nitric-oxide synthase in plant peroxisomes. J. Biol. Chem. 274, 36729 36733. Available from: https://doi.org/ 10.1074/jbc.274.51.36729.

Plant Life under Changing Environment

804

32. Role of nitric oxide dependent posttranslational modifications of proteins under abiotic stress

Barroso, J.B., Corpas, F.J., Carreras, A., Rodrı´guez-Serrano, M., Esteban, F.J., Ferna´ndez-Ocan˜a, A., et al., 2006. Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J. Exp. Bot. 57, 1785 1793. Available from: https://doi.org/10.1093/jxb/erj175. Batthyany, C., Schopfer, F.J., Baker, P.R.S., Dura´n, R., Baker, L.M.S., Huang, Y., et al., 2006. Reversible post-translational modification of proteins by nitrated fatty acids in vivo. J. Biol. Chem. 281 (29), 20450 20463. Begara-Morales, J.C., Chaki, M., Sa´nchez-Calvo, B., Mata-Pe´rez, C., Leterrier, M., Palma, J.M., et al., 2013. Protein tyrosine nitration in pea roots during development and senescence. J. Exp. Bot. 64, 1121 1134. Available from: https://doi.org/10.1093/jxb/ert006. Begara-Morales, J.C., Sa´nchez-Calvo, B., Chaki, M., Valderrama, R., Mata-Pe´rez, C., Lo´pez-Jaramillo, J., et al., 2014a. Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J. Exp. Bot. 65, 527 538. Available from: https://doi.org/10.1093/jxb/ert396. Begara-Morales, J.C., Sa´nchez-Calvo, B., Luque, F., Leyva-Pe´rez, M.O., Leterrier, M., Corpas, F.J., et al., 2014b. Differential transcriptomic analysis by RNA-seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol. 55, 1080 1095. Available from: https://doi.org/10.1093/pcp/pcu044. Begara-Morales, J.C., Sa´nchez-Calvo, B., Chaki, M., Mata-Pe´rez, C., Valderrama, R., Padilla, M.N., et al., 2015. Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J. Exp. Bot. 66, 5983 5996. Available from: https://doi.org/10.1093/jxb/erv306. Benhar, M., Stamler, J.S., 2005. A central role for S-nitrosylation in apoptosis. Nat. Cell Biol. 7, 645 646. Available from: https://doi.org/10.1038/ncb0705-645. Besson-Bard, A., Pugin, A., Wendehenne, D., 2008. New insights into nitric oxide signaling in plants. Annu. Rev. Plant. Biol. 59, 21 39. Available from: https://doi.org/10.1146/annurev.arplant.59.032607.092830. Bethke, P.C., Gubler, F., Jacobsen, J.V., Jones, R.L., 2004. Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta 219, 847 855. Available from: https://doi.org/10.1007/s00425-004-1282-x. Boyer, J.S., 1982. Plant productivity and environment. Science (80-.) 218, 443 448. Available from: https://doi. org/10.1126/science.218.4571.443. Camejo, D., Romero-Puertas, M., del, C., Rodrı´guez-Serrano, M., Sandalio, L.M., La´zaro, J.J., et al., 2013. Salinityinduced changes in S-nitrosylation of pea mitochondrial proteins. J. Proteomics 79, 87 99. Available from: https://doi.org/10.1016/j.jprot.2012.12.003. Camejo, D., Ortiz-Espı´n, A., La´zaro, J.J., Romero-Puertas, M.C., La´zaro-Payo, A., Sevilla, F., et al., 2015. Functional and structural changes in plant mitochondrial PrxII F caused by NO. J. Proteomics 119, 112 125. Available from: https://doi.org/10.1016/j.jprot.2015.01.022. Chaki, M., Ferna´ndez-Ocan˜a, A.M., Valderrama, R., Carreras, A., Esteban, F.J., Luque, F., et al., 2009a. Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant Cell Physiol. 50, 265 279. Available from: https://doi.org/10.1093/pcp/pcn196. Chaki, M., Valderrama, R., Ferna´ndez-Ocan˜a, A.M., Carreras, A., Lo´pez-Jaramillo, J., Luque, F., et al., 2009b. Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J. Exp. Bot. 60, 4221 4234. Available from: https://doi.org/10.1093/jxb/erp263. Chaki, M., Valderrama, R., Ferna´ndez-Ocan˜a, A.M., Carreras, A., Go´mez-Rodrı´guez, M.V., Lo´pez-Jaramillo, J., et al., 2011a. High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ. 34, 1803 1818. Available from: https://doi.org/10.1111/j.1365-3040.2011.02376.x. Chaki, M., Valderrama, R., Ferna´ndez-Ocan˜a, A.M., Carreras, A., Go´mez-Rodrı´guez, M.V., Pedrajas, J.R., et al., 2011b. Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J. Exp. Bot. 62, 1803 1813. Available from: https://doi.org/10.1093/jxb/erq358. Chaki, M., Carreras, A., Lo´pez-Jaramillo, J., Begara-Morales, J.C., Sa´nchez-Calvo, B., Valderrama, R., et al., 2013. Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (β-CA) activity under high temperature stress. Nitric Oxide Biol. Chem. 29, 30 33. Available from: https://doi.org/10.1016/j.niox.2012.12.003. Chaki, M., Kovacs, I., Spannagl, M., Lindermayr, C., 2014. Computational prediction of candidate proteins for S-nitrosylation in Arabidopsis thaliana. PLoS One 9. Available from: https://doi.org/10.1371/journal. pone.0110232. Chaki, M., Shekariesfahlan, A., Ageeva, A., Mengel, A., von Toerne, C., Durner, J., et al., 2015. Identification of nuclear target proteins for S-nitrosylation in pathogen-treated Arabidopsis thaliana cell cultures. Plant Sci. 238, 115 126. Available from: https://doi.org/10.1016/j.plantsci.2015.06.011.

Plant Life under Changing Environment

References

805

Chaves, M.M., Flexas, J., Pinheiro, C., 2009. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot. Available from: https://doi.org/10.1093/aob/mcn125. Chen, Y.J., Ku, W.C., Lin, P.Y., Chou, H.C., Khoo, K.H., Chen, Y.J., 2010. S-Alkylating labeling strategy for sitespecific identification of the S-nitrosoproteome. J. Proteome Res. 9, 6417 6439. Available from: https://doi. org/10.1021/pr100680a. Clark, D., Durner, J., Navarre, D.A., Klessig, D.F., 2000. Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol. Plant Microbe Interact. 13, 1380 1384. Available from: https://doi.org/10.1094/ MPMI.2000.13.12.1380. Corpas, F.J., Barroso, J.B., 2013. Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol. Available from: https://doi.org/10.1111/nph.12380. Corpas, F.J., Barroso, J.B., 2014. Peroxynitrite (ONOO2) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Ann. Bot. 113, 87 96. Available from: https://doi.org/10.1093/ aob/mct260. Corpas, F.J., del Rı´o, L.A., Barroso, J.B., 2007. Need of biomarkers of nitrosative stress in plants. Trends Plant Sci. Available from: https://doi.org/10.1016/j.tplants.2007.08.013. Corpas, F.J., Chaki, M., Ferna´ndez-Ocan˜a, A., Valderrama, R., Palma, J.M., Carreras, A., et al., 2008. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol. 49, 1711 1722. Available from: https://doi.org/10.1093/pcp/pcn144. Corpas, F.J., Hayashi, M., Mano, S., Nishimura, M., Barroso, J.B., 2009. Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol. 151, 2083 2094. Available from: https://doi.org/10.1104/pp.109.146100. Corpas, F.J., Leterrier, M., Valderrama, R., Airaki, M., Chaki, M., Palma, J.M., et al., 2011. Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci. Available from: https://doi.org/ 10.1016/j.plantsci.2011.04.005. Corpas, F.J., Leterrier, M., Begara-Morales, J.C., Valderrama, R., Chaki, M., Lo´pez-Jaramillo, J., et al., 2013a. Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration. Biochim. Biophys. Acta Gen. Subj. 1830, 4981 4989. Available from: https://doi.org/10.1016/j.bbagen.2013.07.002. Corpas, F.J., Palma, J.M., del Rı´o, L.A., Barroso, J.B., 2013b. Protein tyrosine nitration in higher plants grown under natural and stress conditions. Front. Plant Sci. 4. Available from: https://doi.org/10.3389/fpls.2013.00029. Corpas, F.J., Begara-morales, J.C., Sa´nchez-Calvo, B., Chaki, M., Barroso, J.B., 2015. Nitration and S-Nitrosylation: two post-translational modifications (PTMs) mediated by reactive nitrogen species (RNS) and their role in signalling processes of plant cells. In: Gupta, K., Igamberdiev, A. (Eds.), Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants. Signaling and Communication in Plants, vol. 23. Springer, Cham, pp. 267 281. David, A., Yadav, S., Baluˇska, F., Bhatla, S.C., 2015. Nitric oxide accumulation and protein tyrosine nitration as a rapid and long distance signalling response to salt stress in sunflower seedlings. Nitric Oxide Biol. Chem. 50, 28 37. Available from: https://doi.org/10.1016/j.niox.2015.08.003. De Michele, R., Vurro, E., Rigo, C., Costa, A., Elviri, L., Di Valentin, M., et al., 2009. Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol. 150, 217 228. Available from: https://doi.org/10.1104/pp.108.133397. Du, J., Li, M., Kong, D., Wang, L., Lv, Q., Wang, J., et al., 2014. Nitric oxide induces cotyledon senescence involving co-operation of the NES1/MAD1 and EIN2-associated ORE1 signalling pathways in Arabidopsis. J. Exp. Bot. 65, 4051 4063. Available from: https://doi.org/10.1093/jxb/ert429. Durner, J., Wendehenne, D., Klessig, D.F., 1998. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. U.S.A. 95, 10328 10333. Available from: https://doi.org/10.1073/pnas.95.17.10328. Fancy, N.N., Bahlmann, A.-K., Loake, G.J., 2016. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 1 11. Available from: https://doi.org/10.1111/pce.12707. Fares, A., Rossignol, M., Peltier, J.B., 2011. Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem. Biophys. Res. Commun. 416, 331 336. Available from: https://doi.org/10.1016/j.bbrc.2011.11.036. Fares, S., Vargas, R., Detto, M., Goldstein, A.H., Karlik, J., Paoletti, E., et al., 2013. Tropospheric ozone reduces carbon assimilation in trees: estimates from analysis of continuous flux measurements. Global Change Biol. 19, 2427 2443. Available from: https://doi.org/10.1111/gcb.12222. Fazzari, M., Trostchansky, A., Schopfer, F.J., Salvatore, S.R., Sa´nchez-Calvo, B., Vitturi, D., et al., 2014. Olives and olive oil are sources of electrophilic fatty acid nitroalkenes. PLoS One 9. Available from: https://doi.org/ 10.1371/journal.pone.0084884.

Plant Life under Changing Environment

806

32. Role of nitric oxide dependent posttranslational modifications of proteins under abiotic stress

´ ., O ´ ., et al., 2016. Different zinc sensitivity of ¨ rdo¨g, A., Borde´, A Feigl, G., Kolbert, Z., Lehotai, N., Molna´r, A Brassica organs is accompanied by distinct responses in protein nitration level and pattern. Ecotoxicol. Environ. Saf. 125, 141 152. Available from: https://doi.org/10.1016/j.ecoenv.2015.12.006. Fernando Reyes, L., Emilio Villarreal, J., Cisneros-Zevallos, L., 2006. The increase in antioxidant capacity after wounding depends on the type of fruit or vegetable tissue. Food Chem. 101, 1254 1262. Available from: https://doi.org/10.1016/j.foodchem.2006.03.032. Freeman, B.A., Baker, P.R.S., Schopfer, F.J., Woodcock, S.R., Napolitano, A., D’Ischia, M., 2008. Nitro-fatty acid formation and signaling. J. Biol. Chem. Available from: https://doi.org/10.1074/jbc.R800004200. Gaupels, F., Furch, A.C.U., Zimmermann, M.R., Chen, F., Kaever, V., Buhtz, A., et al., 2016. Corrigendum: systemic induction of NO-, Redox-, and cGMP signaling in the pumpkin extrafascicular phloem upon local leaf wounding. Front. Plant Sci. 7. Available from: https://doi.org/10.3389/fpls.2016.00281. Geisler, A.C., Rudolph, T.K., 2012. Nitroalkylation a redox sensitive signaling pathway. Biochim. Biophys. Acta Gen. Subj. Available from: https://doi.org/10.1016/j.bbagen.2011.06.014. Guo, F.-Q., Crawford, N.M., 2005. Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17, 3436 3450. Available from: https:// doi.org/10.1105/tpc.105.037770. Gupta, K.J., 2011. Protein S-nitrosylation in plants: photorespiratory metabolism and NO signaling. Sci. Signal. Available from: https://doi.org/10.1126/scisignal.2001404. Gupta, D.K., Huang, H.G., Corpas, F.J., 2013. Lead tolerance in plants: strategies for phytoremediation. Environ. Sci. Pollut. Res. Available from: https://doi.org/10.1007/s11356-013-1485-4. Hao, G., Derakhshan, B., Shi, L., Campagne, F., Gross, S.S., 2006. SNOSID, a proteomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures. Proc. Natl. Acad. Sci. U.S.A. 103, 1012 1017. Available from: https://doi.org/10.1073/pnas.0508412103. Hasegawa, P.M., Bressan, R.A., Zhu, J.-K., Bohnert, H.J., 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 51, 463 499. Available from: https://doi.org/10.1146/ annurev.arplant.51.1.463. He, Y., Tang, R.H., Hao, Y., Stevens, R.D., Cook, C.W., Ahn, S.M., et al., 2004. Nitric oxide represses the Arabidopsis floral transition. Science (80-.) 305, 1968 1971. Available from: https://doi.org/10.1126/ science.1098837. Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E., Stamler, J.S., 2005. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. Available from: https://doi.org/10.1038/nrm1569. Hu, J., Huang, X., Chen, L., Sun, X., Lu, C., Zhang, L., et al., 2015. Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol. 167, 1731 1746. Available from: https:// doi.org/10.1104/pp.15.00026. Jaffrey, S.R., Snyder, S.H., 2001. The biotin switch method for the detection of S-nitrosylated proteins. Sci. Signal. 2001, pl1. Available from: https://doi.org/10.1126/stke.2001.86.pl1. Kangasja¨rvi, J., Jaspers, P., Kollist, H., 2005. Signalling and cell death in ozone-exposed plants. Plant Cell Environ. Available from: https://doi.org/10.1111/j.1365-3040.2005.01325.x. Kra¨mer, U., Clemens, S., 2005. Molecular biology of metal homeostasis and detoxification. In: Tama¨s, M., Martinoia, E. (Eds.), Topics in Current Genetics. Springer Verlag, New York, pp. 216 271. Langebartels, C., Wohlgemuth, H., Kschieschan, S., Gru¨n, S., Sandermann, H., 2002. Oxidative burst and cell death in ozone-exposed plants. Plant Physiol. Biochem 40 (6-8), 567 575. Available from: https://doi.org/ 10.1016/S0981-9428(02)01416-X. Larkindale, J., Vierling, E., 2007. Core genome responses involved in acclimation to high temperature. Plant Physiol. 146, 748 761. Available from: https://doi.org/10.1104/pp.107.112060. Lee, U., Wie, C., Fernandez, B.O., Feelisch, M., Vierling, E., 2008. Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20, 786 802. Available from: https://doi.org/10.1105/tpc.107.052647. Lee, T.Y., Chen, Y.J., Lu, T.C., Huang, H., Da, Chen, Y.J., 2011. Snosite: exploiting maximal dependence decomposition to identify cysteine S-nitrosylation with substrate site specificity. PLoS One 6. Available from: https:// doi.org/10.1371/journal.pone.0021849. Leo´n, J., Rojo, E., Sa´nchez-Serrano, J.J., 2001. Wound signalling in plants. J. Exp. Bot. Available from: https://doi. org/10.1093/jxb/52.354.1.

Plant Life under Changing Environment

References

807

Leterrier, M., Airaki, M., Palma, J.M., Chaki, M., Barroso, J.B., Corpas, F.J., 2012. Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ. Pollut. 166, 136 143. Available from: https://doi.org/10.1016/j.envpol.2012.03.012. Lindermayr, C., Durner, J., 2009. S-Nitrosylation in plants: pattern and function. J. Proteomics 73, 1 9. Available from: https://doi.org/10.1016/j.jprot.2009.07.002. Lindermayr, C., Saalbach, G., Durner, J., 2005. Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol. 137, 921 930. doi:pp. 104.058719 [pii]\r10.1104/pp. 104.058719. Lin, A., Wang, Y., Tang, J., Xue, P., Li, C., Liu, L., et al., 2012. Nitric oxide and protein s-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol. 158, 451 464. Mata-Pe´rez, C., Begara-Morales, J.C., Chaki, M., Sa´nchez-Calvo, B., Valderrama, R., Padilla, M.N., et al., 2016a. Protein tyrosine nitration during development and abiotic stress response in plants. Front. Plant Sci. 7, 1699. Available from: https://doi.org/10.3389/fpls.2016.01699. Mata-Pe´rez, C., Sa´nchez-Calvo, B., Padilla, M.N., Begara-Morales, J.C., Luque, F., Melguizo, M., et al., 2016b. Nitro-fatty acids in plant signaling: nitro-linolenic acid induces the molecular chaperone network in Arabidopsis. Plant Physiol. 170, 686 701. Available from: https://doi.org/10.1104/pp.15.01671. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M.A., Shulaev, V., et al., 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2. Available from: https://doi.org/10.1126/scisignal.2000448. Mittler, R., 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15 19. Available from: https://doi.org/10.1016/j.tplants.2005.11.002. Neill, S.J., Desikan, R., Clarke, A., Hancock, J.T., 2002. Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128, 13 16. Available from: https://doi.org/10.1104/pp.010707. shown. Ortega-Galisteo, A.P., Rodrı´guez-Serrano, M., Pazmin˜o, D.M., Gupta, D.K., Sandalio, L.M., Romero-Puertas, M.C., 2012. S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J. Exp. Bot. 63, 2089 2103. Available from: https://doi.org/10.1093/jxb/err414. Padilla, M.N., Mata-Pe´rez, C., Melguizo, M., Barroso, J.B., 2017. In vitro nitro-fatty acid release from Cys-NO2fatty acid adducts under nitro-oxidative conditions. Nitric Oxide. 68, 14 22. Available from: https://doi.org/ 10.1016/j.niox. Pal, R., Rai, J.P.N., 2010. Phytochelatins: peptides involved in heavy metal detoxification. Appl. Biochem. Biotechnol. Available from: https://doi.org/10.1007/s12010-009-8565-4. Puyaubert, J., Fares, A., Re´ze´, N., Peltier, J.B., Baudouin, E., 2014. Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: effect of cold stress on cysteine nitrosylation level. Plant Sci. 215 216, 150 156. Available from: https://doi.org/10.1016/j.plantsci.2013.10.014. Qiao, W., Fan, L.-M., 2008. Nitric oxide signaling in plant responses to abiotic stresses. J. Integr. Plant Biol. 50, 1238 1246. Available from: https://doi.org/10.1111/j.1744-7909.2008.00759.x. Radi, R., 2013. Peroxynitrite, a Stealthy Biological Oxidant. J. Biol. Chem. 288 (37), 26464 26472. Available from: https://doi.org/10.1074/jbc.R113.472936. Romero-Puertas, M.C., Campostrini, N., Matte`, A., Righetti, P.G., Perazzolli, M., Zolla, L., et al., 2008. Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Plant Proteomics. 8 (7), 1459 1469. Available from: https://doi.org/10.1002/pmic.200700536. Rubbo, H., 2013. Nitro-fatty acids: novel anti-inflammatory lipid mediators. Braz. J. Med. Biol. Res. Available from: https://doi.org/10.1590/1414-431X20133202. Rudolph, V., Rudolph, T.K., Schopfer, F.J., Bonacci, G., Woodcock, S.R., Cole, M.P., et al., 2010. Endogenous generation and protective effects of nitro-fatty acids in a murine model of focal cardiac ischaemia and reperfusion. Cardiovasc. Res. 85, 155 166. Available from: https://doi.org/10.1093/cvr/cvp275. Schopfer, F.J., Baker, P.R., Freeman, B.A., 2003. NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response? Trends Biochem. Sci. 28 (12), 646 654. Schopfer, F.J., Cipollina, C., Freeman, B.A., 2011. Formation and signaling actions of electrophilic lipids. Chem. Rev. Available from: https://doi.org/10.1021/cr200131e. Sehrawat, A., Abat, J.K., Deswal, R., 2013. RuBisCO depletion improved proteome coverage of cold responsive Snitrosylated targets in Brassica juncea. Front. Plant Sci. 4. Available from: https://doi.org/10.3389/ fpls.2013.00342.

Plant Life under Changing Environment

808

32. Role of nitric oxide dependent posttranslational modifications of proteins under abiotic stress

Shinozaki, K., Yamaguchi-Shinozaki, K., Seki, M., 2003. Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant. Biol. Available from: https://doi.org/10.1016/S1369-5266(03)00092-X. Stamler, J.S., Lamas, S., Fang, F.C., 2001. Nitrosylation: the prototypic redox-based signaling mechanism. Cell 675 683. Available from: https://doi.org/10.1016/S0092-8674(01)00495-0. Stratmann, J.W., 2003. Long distance run in the wound response jasmonic acid is pulling ahead. Trends Plant Sci. Available from: https://doi.org/10.1016/S1360-1385(03)00106-7. Suzuki, N., Mittler, R., 2006. Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol. Plant. Available from: https://doi.org/10.1111/j.0031-9317.2005.00582.x. Taldone, F.S., Tummala, M., Goldstein, E.J., Ryzhov, V., Ravi, K., Black, S.M., 2005. Studying the S-nitrosylation of model peptides and eNOS protein by mass spectrometry. Nitric Oxide Biol. Chem. 13, 176 187. Available from: https://doi.org/10.1016/j.niox.2005.06.004. Tanou, G., Job, C., Rajjou, L., Arc, E., Belghazi, M., Diamantidis, G., et al., 2009. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J. 60, 795 804. Available from: https://doi.org/10.1111/j.1365-313X.2009.04000.x. Tanou, G., Filippou, P., Belghazi, M., Job, D., Diamantidis, G., Fotopoulos, V., et al., 2012. Oxidative and nitrosativebased signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J. 72, 585 599. Available from: https://doi.org/10.1111/j.1365-313X.2012.05100.x. Torta, F., Usuelli, V., Malgaroli, A., Bachi, A., 2008. Proteomic analysis of protein S-nitrosylation. Proteomics. Available from: https://doi.org/10.1002/pmic.200800089. Vainonen, J.P., Kangasja¨rvi, J., 2015. Plant signalling in acute ozone exposure. Plant Cell Environ. Available from: https://doi.org/10.1111/pce.12273. Valderrama, R., Corpas, F.J., Carreras, A., Go´mez-Rodrı´guez, M.V., Chaki, M., Pedrajas, J.R., et al., 2006. The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant Cell Environ. 29, 1449 1459. Available from: https://doi.org/10.1111/j.13653040.2006.01530.x. Valderrama, R., Corpas, F.J., Carreras, A., Ferna´ndez-Ocan˜a, A., Chaki, M., Luque, F., et al., 2007. Nitrosative stress in plants. FEBS Lett. 581, 453 461. Available from: https://doi.org/10.1016/j.febslet.2007.01.006. Vanzo, E., Ghirardo, A., Merl-Pham, J., Lindermayr, C., Heller, W., Hauck, S.M., et al., 2014. S-Nitroso-proteome in poplar leaves in response to acute ozone stress. PLoS One 9. Available from: https://doi.org/10.1371/journal.pone.0106886. Vanzo, E., Merl-Pham, J., Velikova, V., Ghirardo, A., Lindermayr, C., Hauck, S.M., et al., 2016. Modulation of protein S-nitrosylation by isoprene emission in poplar. Plant Physiol. 170, 1945 1961. Available from: https:// doi.org/10.1104/pp.15.01842. Villacorta, L., Gao, Z., Schopfer, F.J., Freeman, B.A., Chen, Y.E., 2016. Nitro-fatty acids in cardiovascular regulation and diseases: characteristics and molecular mechanisms. Front. Biosci. (Landmark Ed.) 21, 873 889. Volkov, R.A., Panchuk, I.I., Mullineaux, P.M., Scho¨ffl, F., 2006. Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol. Biol. 61, 733 746. Available from: https://doi.org/ 10.1007/s11103-006-0045-4. Wang, Y., Yun, B.W., Kwon, E.J., Hong, J.K., Yoon, J., Loake, G.J., 2006. S-Nitrosylation: an emerging redox-based post-translational modification in plants. J. Exp. Bot. 57 (8), 1777 1784. Available from: https://doi.org/ 10.1093/jxb/erj211. Wang, W., Vinocur, B., Shoseyov, O., Altman, A., 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244 252. Available from: https://doi.org/10.1016/ j.tplants.2004.03.006. Wisastra, R., Poelstra, K., Bischoff, R., Maarsingh, H., Haisma, H.J., Dekker, F.J., 2011. Antibody-free detection of protein tyrosine nitration in tissue sections. ChemBioChem 12, 2016 2020. Available from: https://doi.org/ 10.1002/cbic.201100148. Xu, Y., Ding, J., Wu, L.Y., Chou, K.C., 2013a. iSNO-PseAAC: predict cysteine S-nitrosylation sites in proteins by incorporating position specific amino acid propensity into pseudo amino acid composition. PLoS One 8. Available from: https://doi.org/10.1371/journal.pone.0055844. Xu, Y., Shao, X.-J., Wu, L.-Y., Deng, N.-Y., Chou, K.-C., 2013b. iSNO-AAPair: incorporating amino acid pairwise coupling into PseAAC for predicting cysteine S-nitrosylation sites in proteins. PeerJ 1, e171. Available from: https://doi.org/10.7717/peerj.171.

Plant Life under Changing Environment

Further reading

809

Xue, Y., Liu, Z., Gao, X., Jin, C., Wen, L., Yao, X., et al., 2010. GPS-SNO: computational prediction of protein Snitrosylation sites with a modified GPS algorithm. PLoS One 5, 1 7. Available from: https://doi.org/10.1371/ journal.pone.0011290. Ziogas, V., Tanou, G., Filippou, P., Diamantidis, G., Vasilakakis, M., Fotopoulos, V., et al., 2013. Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol. Biochem. 68, 118 126. Available from: https://doi.org/10.1016/j.plaphy.2013.04.004.

Further reading Ainsworth, E.A., Rogers, A., Leakey, A.D.B., 2008. Targets for crop biotechnology in a future high-CO2 and highO3 world. Plant Physiol. 147, 13 19. Available from: https://doi.org/10.1104/pp.108.117101.

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C H A P T E R

33 Regulatory role of circadian clocks in plant responses to abiotic stress Mohamed A. El-Esawi1 and Ibrahim M. Abdelsalam2 1

Botany Department, Faculty of Science, Tanta University, Tanta, Egypt 2Alnoor Laboratory, Qotour, Egypt

33.1 Introduction Development of crops with improved abiotic stress resistance is increasingly required (Grundy et al., 2015). However, mechanisms mediating the abiotic factors affecting plants should be understood to enhance the resistance to such conditions. Environmental stress can pose a serious threat to cellular homeostasis through various processes (Grundy et al., 2015). For example, cold temperatures can cause detrimental problems for the cell such as dehydration and perturbation of plasma membrane (Pearce, 2001; Yamazaki et al., 2009; Grundy et al., 2015). Various transgenic lines with enhanced abiotic stress tolerance have been developed in different crop varieties, and a few number of these have been commercially exploited (Waltz, 2014; Cabello et al., 2014; Grundy et al., 2015). Many transgenes can also be utilized by such transgenic lines to maintain osmotic regulation under environmental stresses. For instance, Nemali et al. (2014) transformed Monsanto’s DroughtGard maize (MON87460) with CspB protein to enhance water capacity under water deficit conditions (Grundy et al., 2015). Osmotin was utilized for improving resistance to salt stress in tomato, cotton, chili pepper, and strawberry (Subramanyam et al., 2010; Parkhi et al., 2009; Patade et al., 2013; Grundy et al., 2015). Circadian clock allows the living organism to predict properly the diurnal fluctuations of the earth’s cycle and are found in various organisms such as insects, fungi, cyanobacteria, and mammals (Grundy et al., 2015). Moreover, it is demonstrated that circadian clocks are not necessary for plant survival or development of arrhythmic mutants, but wellturned clocks can contribute largely to plant growth and fitness under diurnal light and darkness cycles (Grundy et al., 2015). For instance, optimum starch utilization could be attained at night by a clock with preventing starvation before dawn (Scialdone et al., 2013; Webb and Satake, 2015; Grundy et al., 2015). In addition, the circadian clock improves

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plant resistance to abiotic factors, and this subsequently contributes to the plant fitness (Grundy et al., 2015). This chapter discusses the important roles of circadian clocks in plant abiotic stress tolerance regulation.

33.2 Role of the circadian clock in regulating plant stress responses Recent reports have demonstrated the important role of circadian clock in mediating stress responses such as high salinity, drought, and freezing stress conditions.

33.2.1 Circadian clock regulates plant response to salt stress Abiotic stress negatively affects plant growth, performance, and development (Vwioko et al., 2017; El-Esawi and Alayafi, 2019a,b; El-Esawi et al., 2017a, 2018a,b,c,d, 2019a,b; Elansary et al., 2017; Elkelish et al., 2019), leading to overproduction of harmful reactive oxygen species (El-Esawi et al., 2015, 2017b; Jourdan et al., 2015; Consentino et al., 2015). Therefore cellular redox state, along with energy supplement, is disturbed by abiotic stress such as high salinity. Hence, the response to such stress is mediated by changing cellular metabolism, architecture, as well as transcriptional programming (Golldack et al., 2014; Seo and Mas, 2015). Several methods have been previously applied to improve plant growth, productivity, and development (El-Esawi and Sammour, 2014; El-Esawi, 2016a,b,c, 2017a,b; El-Esawi et al., 2016a,b, 2017c,d; Elansary et al., 2018). In addition, circadian clock plays important regulatory roles in plant response to salinity stress. The clock component GIGANTEA (GI) functions in maintaining the molecular association between the clock itself and plant tolerance to high salt stress as such component governs the patterns of Salt Overly Sensitive (SOS) expression (Qiu et al., 2002; Kim et al., 2013; Seo and Mas, 2015). The activity of SOS1 antiporter is inhibited by the combining effect of GI and SOS2 kinase (Seo and Mas, 2015). This is accomplished by SOS2 inhibition under nonstressful conditions. In contrast, GI proteolysis is deteriorated by the 26S protesome under high salinity stress. Circadian regulation of GI allows the release of SOS2 as well as the activation of SOS1 when combined with sodium ion sensor (SOS3) (Kim et al., 2013; Seo and Mas, 2015). This leads to further response to salt stress. It is noteworthy that diurnal gating of GI responses is associated with perpetual high salt stress response (Seo and Mas, 2015). Surprisingly, abscisic acid (ABA) clock components are found to be involved in ionic homeostasis. For example, mutations in abar/chlh/ gun5 expression have a major impact on H1-ATPase phosphorylation as well as stabilization of stomatal closure under light conditions (Tsuzuki et al., 2013). Notably, circadian clock properties including amplitude, period, and phase seem to be regulated under salinity (Habte et al., 2014; Kumar et al., 2011; Seo and Mas, 2015). Such regulation pathways are difficult to attain. However, the connection may be promoted through the expression of circadian components, which is regulated directly by abiotic stress responsive cis-elements of the clock genes (Marcolino-Gomes et al., 2014; Habte et al., 2014; Seo and Mas, 2015). In addition, the regulatory pathways are also controlled by various signaling molecules. For example, the combining effect of the circadian system and abiotic stress

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responses is fulfilled through cyclic adenosine diphosphate ribose which is in turn associated intensively with the circadian cycle and is able to regulate the transduction of ABA signaling (Dodd et al., 2007; Seo and Mas, 2015).

33.2.2 Circadian clock regulates plant response to drought stress ABA biosynthesis regulation controls Arabidopsis responsiveness to drought (Seo and Mas, 2015). Most interestingly, rhythmicity of clock genes is displayed under drought stress (Mizuno and Yamashino, 2008; Wilkins et al., 2010; Seo and Mas, 2015). Hence, droughtresponsive pathways are found to be under circadian control. For instance, regulation of cytosolic free [Ca21] is under circadian control and promotes clear oscillations depending on the environmental signals (Dodd et al., 2005; Seo and Mas, 2015). ABA accumulation seems to increase under drought stress and reduce stomatal opening under the same conditions (Seo and Mas, 2015). The stomatal opening shows slight response to ABA at dawn (Hotta et al., 2007), while peaks of ABA response were reported during the afternoon (Correia et al., 1995). This may be in consistent with [Ca21] peak oscillations timing (Seo and Mas, 2015). Transcriptomic analysis of clock-related genes in Arabidopsis revealed the interaction between genes regulating TOC1 and ABA expression (Seo and Mas, 2015). Accordingly, circadian gating of TOC1 was found to be influenced by ABA expression (Legnaioli et al., 2009). Recent findings have reported the relation between TOC1 regulation and ABA signaling using mathematical modeling (Seo and Mas, 2015). It was found that changes in ABA transcription is connected largely to circadian system of TOC1 allowing further rhythmicity of ABA signaling (Pokhilko et al., 2013; Seo and Mas, 2015). Another clock-related gene is PRR7 that is tolerant to drought stress (Liu et al., 2013). PRR7 can regulate a number of genes susceptible to ABA application and drought stress (Seo and Mas, 2015). Stomatal aperture is influenced by triple mutants of PRR9, PRR7, and PRR5 (d975) under stressful and nonstressful growth conditions. This enhances transduction of ABA signaling (Fukushima et al., 2009; Liu et al., 2013; Seo and Mas, 2015). Meanwhile, higher sensitivity to drought stress is maintained by PRR7 overexpressing plants. The clock-related prr7 mutant is more likely to alleviate ABA concentrations (Liu et al., 2013; Seo and Mas, 2015). This suggests that signaling of ABA by TOC1 and PRR7 is carried out via different patterns despite the witnessed contrasts within the levels of TOC1-gated induction (Seo and Mas, 2015). TIME FOR COFFEE (TIC) is a main clock element capable of regulating metabolic stress and signaling under a wide range of environmental stresses (Sanchez-Villarreal et al., 2013; Seo and Mas, 2015). Changes in starch and carbon metabolism are associated with tic mutant expression that affects hypersensitive phenotypes of oxidative stress and ABA (Seo and Mas, 2015). Further response of such mutant to drought stress is promoted by these phenotypes. An osmotic-responsive protein called glycine-rich RNA-binding protein 7 (GRP7) is also more likely to be clock-engaged (Heintzen et al., 1997). In addition, expression of GRP7 acts to mediate stomatal aperture in guard cells (Kim et al., 2008; Seo and Mas, 2015). The accumulation of RD29A and RAB18 is mediated significantly by Grp7 mutant, which also contributes to the tolerance of such genes to osmotic stress and ABA (Cao et al., 2006; Seo and Mas, 2015). Such findings reveal the significant role revealed by the overlapping between the circadian time and environmental conditions in developing clock-associated plant response to drought stress (Seo and Mas, 2015).

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33.2.3 Circadian clock regulates plant response to cold stress Plant tolerance to cold stress is maintained by a process called freezing acclimation in which freezing temperatures are subsequently adapted with the help of nonfreezing conditions (Seo and Mas, 2015). A group of proteins termed C-repeat binding factors (CBFs) proteins are found to be involved in the cold adaptation process. Such proteins play a role in stimulating cold-regulated (COR) transcription (Gilmour et al., 1998), which promotes plant response to high and low temperatures through hormonal homeostasis restoration, metabolic assimilation, and functional protein biosynthesis (Kurepin et al., 2013; Seo and Mas, 2015). It is interesting to note that circadian rhythmicity in many plants reaches its peak by CBF COR transcript and genes exhibiting cold stress responses under diurnal cycles (Fowler et al., 2005; Artlip et al., 2013). Moreover, circadian regulation is possibly mediated by genes other that those responding to ABA and cold stress (Seo and Mas, 2015). The function of such genes is due to their clock-associated elements in their promoters (Dong et al., 2011; Seo and Mas, 2015). In addition, the clock gating can also be integrated into cold-responsive CBF expression with increased rate of expression during the day except for the night when it is prevented (Seo and Mas, 2015). Only plants expressed rhythmically are affected massively by clock-related regulation of cold stress response. This admittedly expresses the role of both proper clock timing and function in the response (Fowler et al., 2005; Seo and Mas, 2015). Apart from CBF expression, the clock gating is found to influence cold-related genes (Dodd et al., 2006; Bieniawska et al., 2008). This opens the possibility for the relation between clock time and its adaptation to cold stresses. Circadian-related components contribute significantly to freezing stress responses (Seo and Mas, 2015). Regulating CBFs and CORs expression under cold stress is suppressed by the mutants cca1-11 and lhy-21 which also acts to inhibit its clock-associated oscillations and thus leads to enhanced freezing responses (Dong et al., 2011; Seo and Mas, 2015). Induction of CBF expression along with their downstream genes are motivated by the triple mutants of d975 at freezing temperatures (Nakamichi et al., 2009; Seo and Mas, 2015). PIF7 and TOC1 were found in association with G-box component of CBF1 and CBF2 promoters. This suppresses their induction during night (Kidokoro et al., 2009). In addition, regulation CBF expression is likely to be responsive to the clock component GIGANTEA (GI) under freezing stress. Hence, gi-3 mutant does not participate in CBF and COR genes assimilation during its tolerance to cold stress (Cao et al., 2005; Seo and Mas, 2015). Osmoticum soluble sugars are also involved in the regulation of freezing-triggered GI responses (Cao et al., 2007). Therefore the response of the circadian clock to freezing stress signaling varies under a wide number of temperature degrees (Seo and Mas, 2015). The activity of circadian components is halted in many plants at freezing temperature (Bieniawska et al., 2008; Ibanez et al., 2008; Seo and Mas, 2015). In addition, the components of freezing-related signaling are capable of adjusting the clock respondent temperature stress. For example, different expressions of nucleocytoplasmic mRNA lengthen the circadian period of hos1 mutants (MacGregor et al., 2013). Furthermore, Cold-responsive LUX transcription is mediated when its promoter binds to CBF1 (Chow et al., 2014; Seo and Mas, 2015). One pathway controlling the transmission of temperature signals to the circadian clock is the alternative splicing (Seo and Mas, 2015). Circadian clock associated 1 (CCA1) and late hypocotyl (LHY) seem to be

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under the influence of temperature-triggered alternative splicing. The variant of CCA1b splice is produced by alternative splicing of the fourth intron maintaining CCA1 (Seo and Mas, 2015). This variant shows scarcity in the DNA-binding MYB domains (Seo and Mas, 2015). However, it contributes to the dimerization mechanism in which CCA1a is combined with LHY (Seo et al., 2012). James et al. (2012) reported that alternative splicing of LHY differs from that of CCA1 as the oscillations of its variant is obtained by nonsense-mediated decay. Notably, the promoter of LHY does not induce the plant adaptation to temperature stress (Seo and Mas, 2015). However, alternative splicing of temperature-related LHY limits the number of developed transcripts under stressful conditions (Seo and Mas, 2015). Moreover, the significant function performed by alternatively spliced components of the clock on temperature stress response is also responsible for changes in the performance of temperature-responsive clock (Seo and Mas, 2015). For example, the pre-mRNA of in a fundamental genome fraction is spliced by one temperature-responsive component of the spliceosome, termed SKIP (Wang et al., 2012). Plants lacking SKIP expression are likely to increase PRR7 and PRR9 transcripts accumulation and lengthen the circadian time of both variants (Seo and Mas, 2015). Another study reveals that snRNP along with LSMs complexes, the major components of the spliceosome, are capable of mediating the clock-related rhythmicity in many plants and mammals (Seo and Mas, 2015). This could be attained by alternative splicing as well as stabilization of clock-regulated components. Future prospects will be directed toward the role of stress-responsive LSMs in alternative splicing of temperature-triggered clock genes (Perez-Santangelo et al., 2014; Seo and Mas, 2015).

33.3 Circadian clock regulates stress-responsive genes Recently, numerous approaches were directed substantially to investigate the molecular mechanisms of circadian clocks in Arabidopsis thaliana, and the results showed that it contain a transcriptional regulatory system. Moreover, CCA1 and LHY transcription factors are expressed at the day start and peak in the early morning (Grundy et al., 2015). Transcription of PRR9, -7, -5, and -1 proteins can lead to downregulation of the LHY and CCA1 genes expression during the afternoon and the night (Nakamichi et al., 2010; Grundy et al., 2015). PRR proteins can inhibit the transcription of LHY/CCA1 in the late night via the expression of three associated proteins termed ELF3, ELF4, and LUX. These proteins form an evening complex which shut down the PRR genes expression and rise the transcription of LHY/CCA1 in the subsequent morning (Onai and Ishiura, 2005; Hazen et al., 2005; Pokhilko et al., 2012; Grundy et al., 2015). A complex of F-box proteins, such as ZTL and LKP2, along with GIGANTEA (GI) can regulate the TOC1 protein light-dependent proteolysis, leading to increasing gene-network oscillations (Kim et al., 2007; Grundy et al., 2015). Mediating central oscillator function depends on input mechanisms regulated by photoreceptors (Somers et al., 1998), whereas a number of output pathways control the clock that regulates different physiological mechanisms (Grundy et al., 2015). Alternations in clock components have an adverse impact on central oscillator function and alter plant tolerance and acclimation to environmental stress conditions (Grundy et al., 2015). For instance, Lai et al. (2012) have demonstrated that mutations in ELF3, LHY, CCA1, ELF4, PRR5, LUX, PRR7, and

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PRR9 make plants hypersensitive to reactive oxygen species (ROS)-generating compounds, while overexpression of CCA1 enhances plant tolerance under abiotic stresses (Grundy et al., 2015). Plants with decreased expression of TOC1 show significantly enhanced tolerance to drought stress (Grundy et al., 2015). However, overexpression of TOC1 results in higher water deficit and decreased survival under the same condition (Legnaioli et al., 2009). prr5,7,9 and toc1 mutants induced plant resistance to cold temperatures (Keily et al., 2013). Such approaches prove the pivotal role of circadian clocks in improving plant tolerance to environmental stresses (Grundy et al., 2015). In Arabidopsis plants, it was found that around 80% of transcription cycle is persistent to light dark or temperature cycles (Edwards et al., 2006; Michael et al., 2008; Covington et al., 2008; Grundy et al., 2015). Several experiments have revealed similar results in other crops such as maize, poplar, rice, soybean, and tomato (Khan et al., 2010; MarcolinoGomes et al., 2014). Significantly, monocot and dicot species are proved to be the conserved parts for the expression of many genes (Filichkin et al., 2011). Based on transcriptomic analyses, it was revealed that the circadian clock controls many abiotic stress responsive genes (Grundy et al., 2015). Hence, heat, osmoticum, or salt are found to be responded by around 50% of Arabidopsis genes (Grundy et al., 2015). Soybean and barley were also reported to have rhythmic expressions of stress-related genes (MarcolinoGomes et al., 2014; Habte et al., 2014; Grundy et al., 2015). This will open new prospects regarding the relation between the daily timing of genes expression and rhythmic fluctuations in environmental conditions (Grundy et al., 2015). Recent observations revealed that abiotic stress-responsive processes were carried out by individual genes expressed across a variety of phases (Grundy et al., 2015). However, maximum level of expression is restricted to certain hours during the day. This shows that these plants are not only capable of responding to diurnal environmental stresses such as heat and cold but also constant condition such as high osmoticum as well as other conditions such as drought (Grundy et al., 2015). Hence, circadian regulations of abiotic stress resistance are a positive strategy for the plant even under constant diurnal conditions.

33.4 Abiotic stress affects clock genes transcription The change in the function of clock genes is an indication of the effect of abiotic stress conditions (Grundy et al., 2015). For instance, high salt stress leads to an increase in the period of circadian regulation in wheat, and expression of clock-regulated genes in barley exceeded at higher levels under osmatic stress (Habte et al., 2014; Grundy et al., 2015). Expression of clock-mediated genes (ELF4, LUX, TOC1, and PRR-like genes) in soybean was reduced under drought stress leading to further disruption in circadian system (Grundy et al., 2015). Expression of LUX and TOC1 increases to higher levels under warm temperatures, whereas CCA1 and LHY RNA rhythmic expression shows a rise at cold temperatures ranging from 17 C to 12 C (Grundy et al., 2015). Furthermore, the circadian period decreases under heat stress (Kusakina et al., 2014), and cold stress, meanwhile, causes reduction in rhythmicity (Grundy et al., 2015). The number of oscillations for clock genes is usually reduced at 4 C during diurnal light and dark cycles and loses its

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rhythmicity under constant light. Only a limited number of clock-associated genes cycling at 20 C oscillated at 4 C under diurnal cycles (Bieniawska et al., 2008; Espinoza et al., 2010). Changes in the regulation of hormone stress responses may cause altered clock function. For example, ACC application of the ethylene (ET) in Arabidopsis, which is the main component for ACC synthesis, reduced the circadian regulation period length, whereas the introduction of salicylic acid (SA) did not affect the period length (Hanano et al., 2006; Grundy et al., 2015). It is well known that decreased CCA1 mRNA levels shortened the period length of the clock in Arabidopsis; however, ABA application increased the period length under low transcription levels of CCA1 mRNA (Grundy et al., 2015). ABREs are found on LHY, and CCA1 promoters which may enhance ABA entry into the clocks (Spensley et al., 2009; Habte et al., 2014; Grundy et al., 2015). Transcription factors mediating stress responses were found to be the main regulators for circadian clock components. For instance, inhibition of PRR7 regulation happens by HsfB2b transcription factor under heat stress (Kolmos et al., 2014), whereas CBF1-binding sites were found on LUX promoter maintaining its circadian regulation under cold stress (Chow and Kay 2013; Grundy et al., 2015). Furthermore, the promoter of CCA1 is repressed by FBH1 transcription factor (Grundy et al., 2015). The expression of such transcription factor is upregulated at high temperatures and downregulated at low temperatures. Expression of CCA1 decreases in FBH1overexpressing plants (Grundy et al., 2015).

33.5 Circadian clock mediates hormone signaling Phytohormones are considered as the main mediators for plant abiotic stress responses (Grundy et al., 2015). One of these phytohormones is ABA which accumulates in large concentrations under water and salinity stress leading to plant response to various stress conditions (Agarwal and Jha, 2010). ABA biosynthesis is also under circadian control. For example, the generation of carotenoid precursors and 9-cis-epoxycarotenoid dioxygenase (NCED) enzyme in Arabidopsis is found to reach its peak in the morning (Covington et al., 2008; Grundy et al., 2015). Also, there is a proportion between the rhythmic transcription of ABA enzymes in maize and the production of ABA in the early morning (Grundy et al., 2015). PRR5, 7, and 9 proteins are major factors controlling rhythmic ABA biosynthesis as their mutants showed enhanced ABA production (Fukushima et al., 2009; Grundy et al., 2015). Stomatal closure is affected significantly by ABA biosynthesis in the afternoon (Grundy et al., 2015). This increases the response of stomatal opening to ABA accumulation (Correia et al., 1995). For example, Legnaioli et al. (2009) overexpressed TOC1 in many plants and found that the plant stomatal opening increased widely under light/ dark cycles; however, reduced expressions of TOC1 lead to stomatal closure (Grundy et al., 2015). TOC1 expression can be regulated by ABAR through the binding of TOC1 to ABAR promoters (Legnaioli et al., 2009; Huang et al., 2012; Grundy et al., 2015). However, the data obtained from ChIP-seq revealed that TOC1 plays a significant role in tolerating ABA biosynthesis (Huang et al., 2012; Grundy et al., 2015). ABA-responsive genes expression is also mediated by circadian clocks (Grundy et al., 2015). For example, approximately 40% of Arabidopsis ABA-responsive genes are regulated by circadian clock (Covington et al., 2008; Grundy et al., 2015). Several hormones contribute to plant abiotic stress

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response including jasmonic acid (JA), SA, ET, but ABA is considered as the most influential hormone in drought and osmotic stress tolerance (Wasternack and Hause, 2013; Cheng et al., 2013; Kazan, 2015; Grundy et al., 2015). Various abiotic stresses including salinity, cold, drought, and heat can be regulated by ET and JA (Grundy et al., 2015). In Arabidopsis and sorghum, ET levels reach its paramount peak during the day and only at evening in potatoes (Chincinska et al., 2013; Grundy et al., 2015). Rhythmicity of ACC SYNTHASE 8 (ACS8) enzyme was found to be the key factor contributing to the rhythmic expression of ET biosynthesis (Thain et al., 2004). Circadian regulation also controls ACS6 gene, as TOC1 can bind to its promoter (Grundy et al., 2015). ACS8 also shows rhythmic expression with two different ACC OXIDASE enzymes (Covington et al., 2008; Grundy et al., 2015). Chincinska et al. (2013) manifested that the rhythmic expression of ET are associated with sucrose transport in potatoes. Therefore mutations in sucrose transporter SUT4 which is expressed rhythmically responds directly to diurnal fluctuations in ET level (Grundy et al., 2015). Downstream signaling of ET is also controlled by the circadian clock which affects XAP5 CIRCADIAN TIMEKEEPER (Grundy et al., 2015). In addition, the regulation of ET signaling including EIN2 and POLARIS is regulated by TOC1 and PRR5 proteins. These proteins also play a pivotal role in encoding ERFs 8 and 5 genes (PLS; Nakamichi et al., 2012; Grundy et al., 2015). SA is known for its developed antioxidative capacity and important role in biotic stress response (Grundy et al., 2015). It is found that SA and JA have an antagonistic effect against pathogen (Spoel et al., 2007). In Arabidopsis, maximum levels of SA could be attained at night (Zhang et al., 2013; Grundy et al., 2015). PHT4;1 is thought to have an adverse impact on SA accumulation. In addition, this gene is believed to influence the oscillation in SA level (Wang et al., 2014). JA expression is found to reach its paramount peak during the midday (Zhang et al., 2013; Grundy et al., 2015). TOC1 protein is the major contributor to rhythmic changes in JA levels as it binds to the promoters of many genes encoding 13-LOX enzymes which are precursors for JA production. TOC1, PRR5, and PRR7 are also the major regulators for JA responses. This involves JASMONATE ZIM DOMAIN or JAZ proteins, which are two negative JA-induced signaling regulators and other factors mediating JA transcription (Nakamichi et al., 2012; Huang et al., 2012; Liu et al., 2013). Nevertheless, a protein called TIC is found to be clock-dependent, and this protein influences the regulation of JA responses (TIC; Shin et al., 2012; Grundy et al., 2015). TIC seems to downregulate JA responses through its association with MYC2, a positive JA signaling respondent which enhances further proteasomal degradation of JA responses (Kazan and Manners, 2013; Grundy et al., 2015). The circadian clock also influences MYC2 mRNA bioaccumulation allowing for rhythmic stimulation of JA responses. Hence, it could be reported that the circadian clock controls massively the patterns of plant hormonal stress responses via regulating production, signaling, and rhythmicity of stress-responsive hormones. ChIP-seq analyses reveal that hormonal signaling components are regulated directly by PRR5, PRR7, and TOC1. However, several studies are still required at genomic level to understand the additional roles displayed by other components of the clock (Grundy et al., 2015). In conclusion, circadian clocks revealed important regulatory roles in plant responses to abiotic stress tolerance.

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References Agarwal, P.K., Jha, B., 2010. Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol. Plant. 54, 201 212. Artlip, T.S., Wisniewski, M.E., Bassett, C.L., Norelli, J.L., 2013. CBF gene expression in peach leaf and bark tissues is gated by a circadian clock. Tree Physiol. 33, 866 877. Bieniawska, Z., Espinoza, C., Schlereth, A., Sulpice, R., Hincha, D.K., Hannah, M.A., 2008. Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol. 147, 263 279. Cabello, J.V., Lodeyro, A.F., Zurbriggen, M.D., 2014. Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr. Opin. Biotechnol. 26, 62 70. Cao, S., Ye, M., Jiang, S., 2005. Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. Plant Cell Rep. 24, 683 690. Cao, S., Jiang, L., Song, S., Jing, R., Xu, G., 2006. AtGRP7 is involved in the regulation of abscisic acid and stress responses in Arabidopsis. Cell. Mol. Biol. Lett. 11, 526 535. Cao, S., Song, Y.Q., Su, L., 2007. Freezing sensitivity in the gigantea mutant of Arabidopsis is associated with sugar deficiency. Biol. Plant. 51, 359 362. Cheng, M.-C., Liao, P.-M., Kuo, W.-W., Lin, T.-P., 2013. The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol. 162, 1566 1582. Chincinska, I., Gier, K., Kru¨gel, U., Liesche, J., He, H., Grimm, B., et al., 2013. Photoperiodic regulation of the sucrose transporter StSUT4 affects the expression of circadian-regulated genes and ethylene production. Front. Plant Sci. 4, 26. Chow, B.Y., Kay, S.A., 2013. Global approaches for telling time: omics and the Arabidopsis circadian clock. Semin. Cell Dev. Biol. 24, 383 392. Chow, B.Y., Sanchez, S.E., Breton, G., Pruneda-Paz, J.L., Krogan, N.T., Kay, S.A., 2014. Transcriptional Regulation of LUX by CBF1 mediates cold input to the circadian clock in Arabidopsis. Curr. Biol. 24, 1518 1524. Consentino, L., Lambert, S., Martino, C., Jourdan, N., Bouchet, P.-E., Witczak, J., et al., 2015. Blue-light dependent reactive oxygen species formation by Arabidopsis cryptochrome may define a novel evolutionarily conserved signalling mechanism. New Phytol. 206, 1450 1462. Correia, M.J., Pereira, J.S., Chaves, M.M., Rodrigues, M.L., Pacheco, C.A., 1995. ABA xylem concentrations determine maximum daily leaf conductance of field-grown Vitis vinifera L. plants. Plant Cell Environ. 18, 511 521. Covington, M.F., Maloof, J.N., Straume, M., Kay, S.A., Harmer, S.L., 2008. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9, R130. Dodd, A.N., Love, J., Webb, A.A., 2005. The plant clock shows its metal: circadian regulation of cytosolic free Ca21. Trends Plant Sci. 10, 15 21. Dodd, A.N., Jakobsen, M.K., Baker, A.J., Telzerow, A., Hou, S.W., Laplaze, L., et al., 2006. Time of day modulates low-temperature Ca signals in Arabidopsis. Plant J. 48, 962 973. Dodd, A.N., Gardner, M.J., Hotta, C.T., Hubbard, K.E., Dalchau, N., Love, J., et al., 2007. The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318, 1789 1792. Dong, M.A., Farre´, E.M., Thomashow, M.F., 2011. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 7241 7246. Edwards, K., Anderson, P., Hall, A., Salathia, N., Locke, J., Lynn, J., et al., 2006. Flowering locus C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18, 639 650. Elansary, H.O., Yessoufou, K., Abdel-Hamid, A.M.E., El-Esawi, M.A., Ali, H.M., Elshikh, M.S., 2017. Seaweed extracts enhance Salam turfgrass performance during prolonged irrigation intervals and saline shock. Front Plant Sci. 8, 830. Elansary, H.O., Szopa, A., Kubica, P., Ekiert, H., Ali, H.M., Elshikh, M.S., et al., 2018. Bioactivities of traditional medicinal plants in Alexandria. Evid. Based Complement. Alternat. Med. 1 13. El-Esawi, M.A., 2016a. Micropropagation technology and its applications for crop improvement. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 523 545.

Plant Life under Changing Environment

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El-Esawi, M.A., 2016b. Nonzygotic embryogenesis for plant development. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 583 598. El-Esawi, M.A., 2016c. Somatic hybridization and microspore culture in Brassica improvement. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 599 609. El-Esawi, M.A., 2017a. Genetic diversity and evolution of Brassica genetic resources: from morphology to novel genomic technologies—a review. Plant Genet Resour. 15, 388 399. El-Esawi, M.A., 2017b. SSR analysis of genetic diversity and structure of the germplasm of faba bean (Vicia faba L.). Comptes Rendus Biol. 340, 474 480. El-Esawi, M.A., Alayafi, A.A., 2019a. Overexpression of rice Rab7 gene improves drought and heat tolerance and increases grain yield in rice (Oryza sativa L.). Genes 10, 56. El-Esawi, M.A., Alayafi, A.A., 2019b. Overexpression of StDREB2 transcription factor enhances drought stress tolerance in Cotton (Gossypium barbadense L.). Genes 10, 142. El-Esawi, M.A., Sammour, R., 2014. Karyological and phylogenetic studies in the genus Lactuca L. (asteraceae). Cytologia 79, 269 275. El-Esawi, M., Glascoe, A., Engle, D., Ritz, T., Link, J., Ahmad, M., 2015. Cellular metabolites modulate in vivo signaling of Arabidopsis cryptochrome-1. Plant Signal. Behav. 10, e1063758. El-Esawi, M.A., Germaine, K., Bourke, P., Malone, R., 2016a. Genetic diversity and population structure of Brassica oleracea germplasm in Ireland using SSR markers. Comptes Rendus Biol. 339, 133 140. El-Esawi, M.A., Germaine, K., Bourke, P., Malone, R., 2016b. AFLP analysis of genetic diversity and phylogenetic relationships of Brassica oleracea in Ireland. Comptes Rendus Biol. 339, 163 170. El-Esawi, M.A., Elansary, H.O., El-Shanhorey, N.A., Abdel-Hamid, A.M.E., Ali, H.M., Elshikh, M.S., 2017a. Salicylic acid-regulated antioxidant mechanisms and gene expression enhance rosemary performance under saline conditions. Front. Physiol. 8, 716. El-Esawi, M., Arthaut, L., Jourdan, N., d’Harlingue, A., Martino, C., Ahmad, M., 2017b. Blue-light induced biosynthesis of ROS contributes to the signaling mechanism of Arabidopsis cryptochrome. Sci. Rep. 7, 13875. El-Esawi, M.A., Elkelish, A., Elansary, H.O., Ali, H.M., Elshikh, M., Witczak, I., et al., 2017c. Genetic transformation and hairy root induction enhance the antioxidant potential of Lactuca serriola L. Oxid. Med. Cell. Longev. 2017, 5604746. El-Esawi, M.A., Mustafa, A., Badr, S., Sammour, R., 2017d. Isozyme analysis of genetic variability and population structure of Lactuca L. germplasm. Biochem. Syst. Ecol. 70, 73 79. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Alayafi, A.A., Witczak, J., Ahmad, M., 2018a. Analysis of genetic variation and enhancement of salt tolerance in French Pea (Pisum sativum L.). Int. J. Mol. Sci. 19, 2433. El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Ali, H.M., Alayafi, A.A., Witczak, J., et al., 2018b. Genetic variation and alleviation of salinity stress in barley (Hordeum vulgare L.). Molecules 23, 2488. El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Alamri, S.A., Ali, H.M., Alayafi, A.A., 2018c. Bacillus firmus (SW5) augments salt tolerance in soybean (Glycine max L.) by modulating root system architecture, antioxidant defense systems and stress-responsive genes expression. Plant Physiol. Biochem. 132, 375 384. El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Alzahrani, S.M., Ali, H.M., Alayafi, A.A., et al., 2018d. Serratia liquefaciens KM4 improves salt stress tolerance in maize by regulating redox potential, ion homeostasis, leaf gas exchange and stress-related gene expression. Int. J. Mol. Sci. 19, 3310. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Alayafi, A.A., 2019a. Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stressrelated genes expression. Environ. Exp. Bot. 159, 55 65. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Ahmad, M., 2019b. Overexpression of AtWRKY30 transcription factor enhances heat and drought stress tolerance in Wheat (Triticum aestivum L.). Genes 10, 163. Espinoza, C., Degenkolbe, T., Caldana, C., Zuther, E., Leisse, A., Willmitzer, L., et al., 2010. Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One 5, e14101. Elkelish, A.A., Soliman, M.H., Alhaithloul, H.A., El-Esawi, M.A., 2019. Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiol. Bioch. 137, 144 153. Filichkin, S.A., Breton, G., Priest, H.D., Dharmawardhana, P., Jaiswal, P., Fox, S.E., et al., 2011. Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules. PLoS One 6, e16907.

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References

821

Fowler, S.G., Cook, D., Thomashow, M.F., 2005. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 137, 961 968. Fukushima, A., Kusano, M., Nakamichi, N., Kobayashi, M., Hayashi, N., Mizuno, T., et al., 2009. Impact of clockassociated Arabidopsis pseudo-response regulators in metabolic coordination. Proc. Natl. Acad. Sci. U.S.A. 106, 7251 7256. Gilmour, S.J., Zarka, D.G., Stockinger, E.J., Salazar, M.P., Houghton, J.M., Thomashow, M.F., 1998. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 16, 433 442. Golldack, D., Li, C., Mohan, H., Probst, N., 2014. Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front. Plant Sci. 5, 151. Grundy, J., Stoker, C., Carre´, I.A., 2015. Circadian regulation of abiotic stress tolerance in plants. Front. Plant Sci. 6, 648. Available from: https://doi.org/10.3389/fpls.2015.00648. Habte, E., Muller, L.M., Shtaya, M., Davis, S.J., Von Korff, M., 2014. Osmotic stress at the barley root affects expression of circadian clock genes in the shoot. Plant Cell Environ. 37, 1321 1327. Hanano, S., Domagalska, M.A., Nagy, F., Davis, S.J., 2006. Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells 11, 1381 1392. Hazen, S.P., Schultz, T.F., Pruneda-Paz, J.L., Borevitz, J.O., Ecker, J.R., Kay, S.A., 2005. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc. Natl. Acad. Sci. U.S.A. 102, 10387 10392. Heintzen, C., Nater, M., Apel, K., Staiger, D., 1997. AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 94, 8515 8520. Hotta, C.T., Gardner, M.J., Hubbard, K.E., Baek, S.J., Dalchau, N., Suhita, D., et al., 2007. Modulation of environmental responses of plants by circadian clocks. Plant Cell Environ. 30, 333 349. Huang, W., Pe´rez-Garcı´a, P., Pokhilko, A., Millar, A.J., Antoshechkin, I., Riechmann, J.L., et al., 2012. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336, 75 79. Ibanez, C., Ramos, A., Acebo, P., Contreras, A., Casado, R., Allona, I., et al., 2008. Overall alteration of circadian clock gene expression in the chestnut cold response. PLoS One 3, e3567. James, A.B., Syed, N.H., Bordage, S., Marshall, J., Nimmo, G.A., Jenkins, G.I., et al., 2012. Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24, 961 981. Jourdan, N., Martino, C., El-Esawi, M., Witczak, J., Bouchet, P.-E., d’Harlingue, A., et al., 2015. Blue light dependent ROS formation by Arabidopsis cryptochrome-2 may contribute towards its signaling role. Plant Signal. Behav. 10, e1042647. Kazan, K., 2015. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci. 20, 219 229. Kazan, K., Manners, J.M., 2013. MYC2: the master in action. Mol. Plant 6, 686 703. Keily, J., Macgregor, D.R., Smith, R.W., Millar, A.J., Halliday, K.J., Penfield, S., 2013. Model selection reveals control of cold signalling by evening-phased components of the plant circadian clock. Plant J. 76, 247 257. Khan, S., Rowe, S., Harmon, F., 2010. Coordination of the maize transcriptome by a conserved circadian clock. BMC Plant Biol. 10, 126. Kidokoro, S., Maruyama, K., Nakashima, K., Imura, Y., Narusaka, Y., Shinwari, Z.K., et al., 2009. The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol. 151, 2046 2057. Kim, W.Y., Fujiwara, S., Suh, S.-S., Kim, J., Kim, Y., Han, L., et al., 2007. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356 360. Kim, J.S., Jung, H.J., Lee, H.J., Kim, K.A., Goh, C.H., Woo, Y., et al., 2008. Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J. 55, 455 466. Kim, W.Y., Ali, Z., Park, H.-J., Park, S.J., Cha, J.-Y., Perez Hormaeche, J., et al., 2013. Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat. Commun. 4, 1352. Kolmos, E., Chow, B.Y., Pruneda-Paz, J.L., Kay, S.A., 2014. HsfB2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock. Proc. Natl. Acad. Sci. U.S.A. 111, 16172 16177. Kumar, K., Rao, K.P., Biswas, D.K., Sinha, A.K., 2011. Rice WNK1 is regulated by abiotic stress and involved in internal circadian rhythm. Plant Signal. Behav. 6, 316 320. Kurepin, L.V., Keshav, P., Dahal, K.P., Savitch, L.V., Singh, J., Bode, R., et al., 2013. Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation. Int. J. Mol. Sci. 14, 12729 12763.

Plant Life under Changing Environment

822

33. Regulatory role of circadian clocks in plant responses to abiotic stress

Kusakina, J., Gould, P.D., Hall, A., 2014. A fast circadian clock at high temperatures is a conserved feature across Arabidopsis accessions and likely to be important for vegetative yield. Plant Cell Environ. 37, 327 340. Lai, A.G., Doherty, C.J., Mueller-Roeber, B., Kay, S.A., Schippers, J.H.M., Dijkwel, P.P., 2012. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc. Natl. Acad. Sci. U.S. A. 109, 17129 17134. Legnaioli, T., Cuevas, J., Mas, P., 2009. TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J. 28, 3745 3757. Liu, T., Carlsson, J., Takeuchi, T., Newton, L., Farre´, E.M., 2013. Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J. 76, 101 114. MacGregor, D.R., Gould, P., Foreman, J., Griffiths, J., Bird, S., Page, R., et al., 2013. HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES1 is required for circadian periodicity through the promotion of nucleocytoplasmic mRNA export in Arabidopsis. Plant Cell 25, 4391 4404. Marcolino-Gomes, J., Rodrigues, F.A., Fuganti-Pagliarini, R., Bendix, C., Nakayama, T.J., Celaya, B., et al., 2014. Diurnal oscillations of soybean circadian clock and drought responsive genes. PLoS One 9, e86402. Michael, T.P., Mockler, T.C., Breton, G., Mcentee, C., Byer, A., Trout, J.D., et al., 2008. Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet. 4, e14. Mizuno, T., Yamashino, T., 2008. Comparative transcriptome of diurnally oscillating genes and hormoneresponsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants. Plant Cell Physiol. 49, 481 487. Nakamichi, N., Kusano, M., Fukushima, A., Kita, M., Ito, S., Yamashino, T., et al., 2009. Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol. 50, 447 462. Nakamichi, N., Kiba, T., Henriques, R., Mizuno, T., Chua, N.H., Sakakibara, H., 2010. PSEUDO-RESPONSE REGULATORS 9,7 and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22, 594 605. Nakamichi, N., Kiba, T., Kamioka, M., Suzuki, T., Yamashino, T., Higashiyama, T., et al., 2012. Transcriptional repressor PRR5 directly regulates clock-output pathways. Proc. Natl. Acad. Sci. U.S.A. 109, 17123 17128. Nemali, K.S., Bonin, C., Dohleman, F.G., Stephens, M., Reeves, W.R., Nelson, D.E., et al., 2014. Physiological responses related to increased grain yield under drought in the first biotechnology-derived drought-tolerant maize. Plant Cell Environ. 38, 1866 1880. Onai, K., Ishiura, M., 2005. PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock. Genes Cells 10, 963 972. Parkhi, V., Kumar, V., Sunilkumar, G., Campbell, L., Singh, N., Rathore, K., 2009. Expression of apoplastically secreted tobacco osmotin in cotton confers drought tolerance. Mol. Breed. 23, 625 639. Patade, V.Y., Khatri, D., Kumari, M., Grover, A., Mohan Gupta, S., Ahmed, Z., 2013. Cold tolerance in osmotin transgenic tomato (Solanum lycopersicum L.) is associated with modulation in transcript abundance of stress responsive genes. Springerplus 2, 117. Pearce, R.S., 2001. Plant freezing and damage. Ann. Bot. 87, 417 424. Perez-Santangelo, S., Mancini, E., Francey, L.J., Schlaen, R.G., Chernomoretz, A., Hogenesch, J.B., et al., 2014. Role for LSM genes in the regulation of circadian rhythms. Proc. Natl. Acad. Sci. U.S.A. 111, 15166 15171. Pokhilko, A., Fernandez, A.P., Edwards, K.D., Southern, M.M., Halliday, K.J., Millar, A.J., 2012. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol. Syst. Biol. 8, 574. Pokhilko, A., Mas, P., Millar, A.J., 2013. Modelling the widespread effects of TOC1 signalling on the plant circadian clock and its outputs. BMC Syst. Biol. 7, 23. Qiu, Q.S., Guo, Y., Dietrich, M.A., Schumaker, K.S., Zhu, J.K., 2002. Regulation of SOS1, a plasma membrane Na1/H1 exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl. Acad. Sci. U.S.A. 99, 8436 8441. Sanchez-Villarreal, A., Shin, J., Bujdoso, N., Obata, T., Neumann, U., Du, S.X., et al., 2013. TIME FOR COFFEE is an essential component in the maintenance of metabolic homeostasis in Arabidopsis thaliana. Plant J. 76, 188 200. Scialdone, A., Mugford, S.T., Feike, D., Skeffington, A., Borrill, P., Graf, A., et al., 2013. Arabidopsis plants perform arithmetic division to prevent starvation at night. Elife 2, e00669. Seo, P.J., Mas, P., 2015. STRESSing the role of the plant circadian clock. Trends Plant Sci. 20, 230 237.

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Seo, P.J., Park, M.J., Lim, M.H., Kim, S.G., Lee, M., Baldwin, I.T., et al., 2012. A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24, 2427 2442. Shin, J., Heidrich, K., Sanchez-Villarreal, A., Parker, J.E., Davis, S.J., 2012. TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis. Plant Cell 24, 2470 2482. Somers, D.E., Devlin, P.F., Kay, S.A., 1998. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282, 1488 1490. Spensley, M., Kim, J.-Y., Picot, E., Reid, J., Ott, S., Helliwell, C., et al., 2009. Evolutionarily conserved regulatory motifs in the promoter of the Arabidopsis clock gene LATE ELONGATED HYPOCOTYL. Plant Cell 21, 2606 2623. Spoel, S.H., Johnson, J.S., Dong, X., 2007. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc. Natl. Acad. Sci. U.S.A. 104, 18842 18847. Subramanyam, K., Sailaja, K.V., Subramanyam, K., Rao, D.M., Lakshmidevi, K., 2010. Ectopic expression of an osmotin gene leads to enhanced salt tolerance in transgenic chilli pepper (Capsicum annum L.). Plant Cell Tissue Organ Cult. 105, 181 192. Thain, S.C., Vandenbussche, F., Laarhoven, L.J., Dowson-Day, M.J., Wang, Z.Y., Tobin, E.M., et al., 2004. Circadian rhythms of ethylene emission in Arabidopsis. Plant Physiol. 136, 3751 3761. Tsuzuki, T., Takahashi, K., Tomiyama, M., Inoue, S.I., Kinoshita, T., 2013. Overexpression of the Mg-chelatase H subunit in guard cells confers drought tolerance via promotion of stomatal closure in Arabidopsis thaliana. Front. Plant Sci. 4, 440. Vwioko, E., Adinkwu, O., El-Esawi, M.A., 2017. Comparative physiological, biochemical and genetic responses to prolonged waterlogging stress in okra and maize given exogenous ethylene priming. Front. Physiol. 8, 632. Waltz, E., 2014. Beating the heat. Nat. Biotechnol. 32, 610 613. Wang, X., Wu, F., Xie, Q., Wang, H., Wang, Y., Yue, Y., et al., 2012. SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 24, 3278 3295. Wang, G., Zhang, C., Battle, S.L., Lu, H., 2014. The phosphate transporter PHT4;1 is a salicylic acid regulator likely controlled by the circadian clock protein CCA1. Front. Plant Sci. 5, 701. Wasternack, C., Hause, B., 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111, 1021 1058. Webb, A.A.R., Satake, A., 2015. Understanding circadian regulation of carbohydrate metabolism in Arabidopsis using mathematical models. Plant Cell Physiol. 56, 586 593. Wilkins, O., Bra¨utigam, K., Campbell, M.M., 2010. Time of day shapes Arabidopsis drought transcriptomes. Plant J. 63, 715 727. Yamazaki, T., Kawamura, Y., Uemura, M., 2009. Extracellular freezing-induced mechanical stress and surface area regulation on the plasma membrane in cold-acclimated plant cells. Plant Signal. Behav. 4, 231 233. Zhang, C., Xie, Q., Anderson, R.G., Ng, G., Seitz, N.C., Peterson, T., et al., 2013. Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog. 9, e1003370.

Further reading Novakova, M., Motyka, V., Dobrev, P.I., Malbeck, J., Gaudinova, A., Vankova, R., 2005. Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves. J. Exp. Bot. 56, 2877 2883.

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C H A P T E R

34 Regulation of genes and transcriptional factors involved in plant responses to abiotic stress Mohamed A. El-Esawi Botany Department, Faculty of Science, Tanta University, Tanta, Egypt

34.1 Introduction Abiotic stress is highly responsible for worldwide crop deficiency which further limits the average productivity of almost all crop plants (Ciarmiello et al., 2011). It also negatively limits plants performance and development (Vwioko et al., 2017; El-Esawi and Alayafi, 2019a,b; El-Esawi et al., 2017a, 2018a,b,c,d, 2019a,b; Elansary et al., 2017), leading to overproduction of harmful reactive oxygen species (ROS) (El-Esawi et al., 2015, 2017b; Jourdan et al., 2015; Consentino et al., 2015). Hence, these plants instantly develop various mechanisms to alleviate toxic effects resulted from environmental stresses (Ciarmiello et al., 2011). Such mechanisms enhance the ability of plants to tolerate the stresses or inhibit their hazardous effects by promoting fixed growth habitus depending on the stress pattern. Plants are found to develop specific responses with metabolic changes during growth and development (Elansary et al., 2018). In addition to the potential use of genetic approaches in improving plant growth, productivity and development (El-Esawi and Sammour, 2014; El-Esawi 2016a,b,c, 2017a,b; El-Esawi et al., 2016a,b, 2017c,d), plantdefense mechanism requires more in depth studies on stress-sensitive precursors and signaling pathways, including protein protein interactions, transcription factors (TFs), and promoters. As a result, different proteins or metabolites are produced (Ciarmiello et al., 2011). In addition, highly toxic ROS can be overproduced under a wide range of abiotic stress conditions including high and low temperatures, daylight stress, osmotic stress, heavy metals, and a number of biotic stresses such as herbicides and toxins (Ciarmiello et al., 2011). One of these ROS is H2O2 which inhibits the photosynthesis process and also cause vigorous cellular damage (Ciarmiello et al., 2011). Hence, antioxidative defense mechanisms function

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can remove ROS quickly. However, removal efficiency is reduced under many stresses which increase their intracellular level leading to an extensive damage (Allan and Fluhr, 2007; Ciarmiello et al., 2011). Plant cells are capable of developing a defense mechanism if they are to inhibit or even alleviate these damages. This mechanism involves the production of antioxidative genes that are highly stress-responsive (Ciarmiello et al., 2011). These genes, in turn, can function by inducing biochemical changes in the plant itself. Recently, several approaches have focused mainly to investigate the regulation system adapted by the plant ion response to stresses (Ciarmiello et al., 2011). The results revealed that this network system is composed of various components including growth-inducing stress-responsive genes, and signaling and regulatory expressive elements (Wang et al., 2003a,b; Ciarmiello et al., 2011). In addition, it is found that plant traits regulating stress responses are substantially quantitative trait loci (QTLs) (Ciarmiello et al., 2011). These traits are difficult to be genetically selected. Furthermore, there are several proteins required during stress response (Ciarmiello et al., 2011). For example, metabolic proteins inducing osmoprotectants production and regulatory protein kinases or transcriptional factors are required for signaling transduction (Ciarmiello et al., 2011).

34.2 Gene regulation and transcriptional factors in plant response to salt stress It is commonly believed that high salinity stress has an enormous impact on cultivated land (Ciarmiello et al., 2011). It disrupts physiological and metabolic processes along with plant growth and development, reducing overall worldwide crop productivity (Ciarmiello et al., 2011). Strained water relation and highly accumulated ions such as Cl2 and, in particular, Na1 in plant cells are the consequences of plant exposure to extreme concentrations of NaCl, which also cause disruption of the other ions’ homeostasis including Ca21, K1, and NO32 (Ciarmiello et al., 2011). Furthermore, high levels of NaCl disrupt various metabolic and physiological processes at different levels, including water deprivation, nutrient disruption, as well as toxicity and oxidative stress (Vinocur and Altman, 2005; Ciarmiello et al., 2011). Hence, plants adapt at least two influential mechanisms to alleviate the negative effects produced such as rapid defense response and long-term tolerance response. Plants develop specific pathways for adaptation response to salinity stress (Ciarmiello et al., 2011). They either induce salt-tolerance effectors to adjust regulatory molecules for signal transduction or adaptation of the function of stress-resistant effector itself (Ciarmiello et al., 2011). Moreover, early and delayed response genes are induced under salinity stress (Sairam and Tyagi, 2004). Expression level of delayed response genes is slow and sustained and is downstream activated by early response genes which are expressed more quickly and transiently (Zhu, 2002; Ciarmiello et al., 2011). Various plants adapt different biochemical mechanisms to induce a wide range of tolerating genes if they are to respond to salinity stress (Ciarmiello et al., 2011). Such mechanisms also play essential roles in other processes such as signal transduction, carbon metabolism, oxidative stress response, synthesis of energy resources, absorption and transport of sodium ions, and also structural modifications in cell walls and membranes (Ciarmiello et al., 2011). In addition, to improve crop productivity, recent approaches have mainly focused on developing genetically engineered plants that exhibit enhanced

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capability to tolerate a variety of stresses (Roy et al., 2011). One approach that is possible to be utilized for such purpose is genetic manipulation either by overexpression or inhibition of specific genes (Roy et al., 2011). Therefore a variety of functional genes are expressed under salinity stress including encoding genes for detoxifying enzymes such as glutathione peroxidase, flavoprotein AtHAL3 (Espinosa-Ruiz et al., 1999), and Alfin1 TF (Bastola et al., 1998; Ciarmiello et al., 2011). Based on transcriptomic analyses, it is reported that transcriptional and translational regulation of synthesized osmolytic-regulated genes and ion transporters such as transcripts of RNA-binding proteins, ribosome-containing genes, and translational factors for initiation and elongation play a significant role in plant adaptation to salt (Sahi et al., 2006; Ciarmiello et al., 2011). Interaction between some TFs such as DRE-specific binding factors, putative zinc finger proteins, bZIP/HD-ZIP-proteins, and MYB proteins (Ciarmiello et al., 2011), and some the promoters of osmolytes can modulate plant salt stress tolerance (Abe et al., 1997; Hasegawa et al., 2000a,b; Ciarmiello et al., 2011). ROS causes damage to protein while interacting nonspecifically with many cellular components (Ciarmiello et al., 2011). Hence, plants adapt enzymatic- and nonenzymatic-related response pathways to counteract ROS production as well as to maintain redox homeostasis. Furthermore, signaling transduction of ROS-regulated MAPK proteins is affected by intracellular ROS, which inhibit phosphatases or downstream TFs (Ciarmiello et al., 2011).

34.3 Regulation of genes and transcriptional factors in plant response to drought stress Plant tolerance to water loss as well as tolerance efficiency is mainly regulated by the genome (Ciarmiello et al., 2011). Arabidopsis thaliana is an example of a model plant that performs microarrays which, in turn, are largely used to regulate the induction or repression of tolerating genes to the conditions of water deprivation (Seki et al., 2002; Ciarmiello et al., 2011). Also, it is necessary to develop more resistant crop varieties to drought stress either by conventional breeding methods or genetic engineering to increase crop productivity worldwide (Roy et al., 2011). Several studies reported the possibility of utilization of genetic transformation in plants to investigate the characteristics of genes involved in the drought-defense mechanism (Roy et al., 2011). Upon stress response, expressed genes can maintain several functions to enhance dehydration tolerance, including protection of the cytoplasm and cell membrane, improving cellular water prospect to enhance water uptake, regulation of ion uptake, and other gene expression (Roy et al., 2011). There are at least four functional groups in which these genes are placed. These functional groups are signal transduction, regulation of transcription process, cellular transport, and structural protection of cellular components (Ciarmiello et al., 2011). Regulating gene expression and/or inhibition is fundamentally controlled by at least six TFs groups under water-deficit stress (Ciarmiello et al., 2011). Several processes are applied to enhance homeobox domain and TFs containing NAC domain ability in response to water deficit (Ciarmiello et al., 2011). Stress tolerance is fulfilled by accumulating structural or metabolic protein groups. Lea genes participate integrally in plant protection (Ciarmiello et al., 2011). These genes are also induced permanently at different

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developmental stages of desiccating seeds. In addition, (Lea) genes play a pivotal role in the synthesis of hydrophilic proteins that, in turn, protect other proteins and membranes via encoding hydrophilic proteins to protect cellular membranes from injuries revealing its role in rice adaptation to environmental stress (Chandra Babu et al., 2004; Ciarmiello et al., 2011). Under water deficit, plants are capable of developing two transcriptional pathways for regulating genetic expression. One of these pathways is mainly controlled by DREB protein which is called ABA-independent pathway (Ciarmiello et al., 2011). DREB protein is found to contain a DNA binding element that is primarily expressed in APETALA2 protein (AP2), (also named flower patterning protein) (Ciarmiello et al., 2011).

34.4 Heavy metal stress and its transcriptional factors regulation Excessive heavy metal uptake by plants is extremely phytotoxic especially when metals accumulate in cells (Brune et al., 1995; Ciarmiello et al., 2011). Plant development is negatively influenced by metal-induced effects which either impair metabolic processes directly and immediately (Van Assche and Clijsters, 1990; Ciarmiello et al., 2011) or induce signaling initiation of adaptation or toxicity responses (Jonak et al., 2004). Defense mechanism driven by plants against heavy metal toxicity involves metal uptake, translocation, and compartmentalization into the vacuole (Meagher, 2000; Ciarmiello et al., 2011). In this context, recent studies have been conducted on A. thaliana as an example of model plant to catalogue tolerating genes to metals. Results showed that Cd treatments were responsible for up- and down-regulation of 65 and 338 genes (Kovalchuk et al., 2005; Ciarmiello et al., 2011). Application of Cd also has the potential to regulate ABC transporters. It helps ABA-containing plants to efficiently transport Cd-binding glutathione and phytochelatins complexes (Ciarmiello et al., 2011; Bovet et al., 2005). In accordance with the hypothesis that short period exposure to heavy metals is the cause of glutathione depletion, it is found that 10 differentially regulated pea genotypes by Cd treatment showed modified relation between glutathione levels and response index (Ciarmiello et al., 2011). Light can alter the photoreceptors localization affecting the activities of photoreceptor itself. One family of angiosperm genes can encode widely known photoreceptor (Phy) (Ciarmiello et al., 2011). There are several consequences of light uptake by plants. Excessive light absorption contributes to the inactivation of phytochemical processes (Karpinski et al., 1999) such as photosynthesis, modification of plastoquinone redox homeostasis, and formation of ROS 1 including H2O2, O2 2 , and O2 (Niyogi, 1999; Ciarmiello et al., 2011). There are different inducers of downstream photoreceptors that are involved in encoding TFs, kinases, phosphatases, as well as degradable proteins (Ciarmiello et al., 2011). These inducers are either specific for light intensity or representing signal-integration points that regulate signaling transduction under high light stress (Ciarmiello et al., 2011). It is found that binding of TFs to promoters is affected by posttranslational phosphorylation of TFs regulating their activities. For instance, TFs can bind to G-box forming fixed GBF1 in absence of phosphorylation (Ciarmiello et al., 2011). However, its affinity to G-box binding increases as CKII

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catalyzes its phosphorylation (Klimczak et al., 1995; Ciarmiello et al., 2011). In response to light, some genes are inducibly regulated by a variety of TFs in the dark.

34.5 Genes and transcriptional factors regulation of chilling and cold stress Cold stress has a negative influence on plant growth especially (Ciarmiello et al., 2011). It also prevents metabolic processes directly causing complete inhibition of plant genetic potential expression. ice1 mutation adversely affects the cold-induced genes that modulate calcium-signaling pathway or encode receptor-specific kinase-related proteins (Ciarmiello et al., 2011). Modifications in the structure of transcriptomes are controlled by a plantregulated proteolysis mechanism under freezing stress (Ciarmiello et al., 2011). Induction of various genes, involved in cellular protection, is regulated by CBFs such as those involved in phosphoinositide and hormone metabolism, membrane ion transport, osmolyte biosynthesis, transcription process, ROS suppression, and signal transduction (Ciarmiello et al., 2011; Lee et al., 2005). DREB1/CBF is widely spread within many higher plants (Ciarmiello et al., 2011). Identification of DREB genes in numerous plants was also reported (Ciarmiello et al., 2011). It is found that several wheat and barley CBF homologs have been involved in QTLs mapping at low temperatures (Va´gu´ifalvi et al., 2005; Ciarmiello et al., 2011).

34.6 Gene regulation of waterlogging tolerance There are a number of changes affecting waterlogged soils such as physical, biological, and chemical changes (Roy et al., 2011). There are several toxic effects on microbes and other microorganisms related to air scarcity in submerged soils, including degradation of organic compounds at a slow rate and through an inefficient way (Roy et al., 2011). This explains the lack of decayed organic matter in waterlogged soils. Genetic engineering technique is of significant importance to be utilized for germplasm amelioration and ensuring the safe various mechanisms applied in response to waterlogging (Roy et al., 2011). Identifying the characteristics of limiting factors tolerating flooding is accomplished by two different approaches (Roy et al., 2011). One participates in downstream expression of single candidate genes such as those involved in ethanol production, whereas the second contributes to upstream expression of TFs. Both techniques have also proven to influence long-range tolerance to oxygen scarcity (Roy et al., 2011). Promoting ethanol production along with threefold PDC-increased activities is mediated more efficiently under anoxic conditions by Taipei 309 driven by a constitutive 35S promoter-binding pdc1 than nontransformed ones (Roy et al., 2011). It is also declared that increasing the rate of ethanol synthesis up to sixfold in many transgenic varieties is compatible with eightfold increase in percentage adaptation tolerance to hypoxia (Qunimio et al., 2000; Roy et al., 2011). However, another study in this regard reported that two transgenic lines of Taipei 309 transferred with pdc1 had over twofold greater PDC activity and 43% improved rate of ethanol production. Adaptive response of lines to anoxic conditions, meanwhile, was less than that of nontransformed controls (Roy et al., 2011). Dennis et al. (2000) reported using

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cDNAs isolated from transgenic cotton plants exhibited 10 13 increased fold in ADH activity and more enhanced rate of ethanol fermentation. Meanwhile, transgenic cotton plants containing pdc1 cDNA linked by a constitutive 35S promoter showed only marginally more PDC activity and produced more PDC protein (Roy et al., 2011). It is perceived that cotton plants with rice ADH only, PDC only, or even both constructs did not support improved adaptation response to hypoxia stress (Roy et al., 2011).

34.7 Transcriptional factors regulation of flooding stress Various plants are found to tolerate flooding for a short time not exceeding few days as these stresses are responsible for anoxic conditions in plant root system (Ciarmiello et al., 2011). Nonphotosynthetic roots depend mainly on mitochondrial respiration to get the energy required for growth. Hence, the respiration process will continue to decrease until the cells die under high oxygen pressure (Bray, 2004; Ciarmiello et al., 2011). Recent experiments have been carried out using a quantitative real-time polymerase chain reaction technique to identify genetically expressed TF families under hypoxic conditions (Scheible et al., 2004; Osuna et al., 2007; Morcuende et al., 2007; Barrero et al., 2009; Ciarmiello et al., 2011). These results revealed that TFs belonging to AP2/ERFtype family along with finger Zinc and basic helix-loop-helix type TFs are recognized as upregulated TFs (Ciarmiello et al., 2011). Various biotic conditions along with abiotic stresses (e.g., absence of oxygen) are the primary cause of excessive concentrations of ROS in plants (Ciarmiello et al., 2011). It is found that at least one of the redox-adaptive TFs is expressed in response to oxygen limitation. In Arabidopsis the signaling network system expresses ZAT12. Based on the analysis of cDNA and genes that contribute efficiently to plant responses to anaerobic conditions, it has been revealed that anaerobically inducible early gene (aie gene) is readily activated by anoxia conditions in rice plants (Ciarmiello et al., 2011).

References Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T., Hosokawa, D., Shinozaki, K., 1997. Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9, 1859 1868. Allan, A.C., Fluhr, R., 2007. Ozone and reactive oxygen species. In: Roberts, K. (Ed.), Handbook of Plant Science. Wiley, Hoboken, NJ, pp. 1229 1304. Barrero, J.M., Millar, A.A., Griffiths, J., Czechowski, T., Scheible, W.R., Udvardi, M., et al., 2009. Gene expression profiling identifies two regulatory genes controlling dormancy and ABA sensitivity in Arabidopsis seeds. Plant J. 61, 611 622. Bastola, D.R., Pethe, V.V., Winicov, I., 1998. A1fin1, a novel zincfinger protein in alfalfa roots that binds to promoter elements in the salt-inducible MsPRP2 gene. Plant Mol. Biol. 38, 1123 1135. Bovet, L., Feller, U., Martinoia, E., 2005. Possible involvement of plant ABC transporters in cadmium detoxification: a cDNA sub-microarray approach. Environ. Int. 31, 263 267. Bray, E.A., 2004. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J. Exp. Bot. 55, 2331 2341. Brune, A., Urbach, W., Dietz, K.J., 1995. Differential toxicity of heavy metals is partly related to a loss of preferential extraplasmic compartmentation: a comparison of Cd-, Mo-, Ni-, and Zn-stress. New Phytol. 129, 404 409.

Plant Life under Changing Environment

References

831

Chandra Babu, R., Jingxian, Z., Blumc, L., David Hod, T.-H., Wue, R., Nguyenf, H.T., 2004. HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci. 166, 855 862. Ciarmiello, L.F., Woodrow, P., Fuggi, A., Pontecorvo, G., Carillo, P., 2011. Plant genes for abiotic stress. In: Shanker, A.K., Venkateswarlu, B. (Eds.), Abiotic Stress in Plants—Mechanisms and Adaptations. InTech, Rijeka, Croatia, pp. 283 308. Consentino, L., Lambert, S., Martino, C., Jourdan, N., Bouchet, P.-E., Witczak, J., et al., 2015. Blue-light dependent reactive oxygen species formation by Arabidopsis cryptochrome may define a novel evolutionarily conserved signalling mechanism. New Phytol. 206, 1450 1462. Dennis, E.S., Dolferus, R., Ellis, M., Rahaman, M., Wu, Y., et al., 2000. Molecular strategies for improving water logging tolerance in plants. J. Exp. Bot. 51, 89 97. Elansary, H.O., Yessoufou, K., Abdel-Hamid, A.M.E., El-Esawi, M.A., Ali, H.M., Elshikh, M.S., 2017. Seaweed extracts enhance salam turfgrass performance during prolonged irrigation intervals and saline shock. Front. Plant Sci. 8, 830. Elansary, H.O., Szopa, A., Kubica, P., Ekiert, H., Ali, H.M., Elshikh, M.S., et al., 2018. Bioactivities of traditional medicinal plants in Alexandria. Evid. Based Complement. Alternat. Med. 1 13. El-Esawi, M.A., 2016a. Micropropagation technology and its applications for crop improvement. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 523 545. El-Esawi, M.A., 2016b. Nonzygotic embryogenesis for plant development. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 583 598. El-Esawi, M.A., 2016c. Somatic hybridization and microspore culture in Brassica improvement. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 599 609. El-Esawi, M.A., 2017a. Genetic diversity and evolution of Brassica genetic resources: from morphology to novel genomic technologies—a review. Plant Genet. Resour. 15, 388 399. El-Esawi, M.A., 2017b. SSR analysis of genetic diversity and structure of the germplasm of faba bean (Vicia faba L.). Comptes Rendus Biol. 340, 474 480. El-Esawi, M.A., Alayafi, A.A., 2019a. Overexpression of Rice Rab7 gene improves drought and heat tolerance and increases grain yield in rice (Oryza sativa L.). Genes 10, 56. El-Esawi, M.A., Alayafi, A.A., 2019b. Overexpression of StDREB2 Transcription Factor Enhances Drought Stress Tolerance in Cotton (Gossypium barbadense L.). Genes 10, 142. El-Esawi, M.A., Sammour, R., 2014. Karyological and phylogenetic studies in the genus Lactuca L. (asteraceae). Cytologia 79, 269 275. El-Esawi, M., Glascoe, A., Engle, D., Ritz, T., Link, J., Ahmad, M., 2015. Cellular metabolites modulate in vivo signaling of Arabidopsis cryptochrome-1. Plant Signal. Behav. 10, e1063758. El-Esawi, M.A., Germaine, K., Bourke, P., Malone, R., 2016a. Genetic diversity and population structure of Brassica oleracea germplasm in Ireland using SSR markers. Comptes Rendus Biol. 339, 133 140. El-Esawi, M.A., Germaine, K., Bourke, P., Malone, R., 2016b. AFLP analysis of genetic diversity and phylogenetic relationships of Brassica oleracea in Ireland. Comptes Rendus Biol. 339, 163 170. El-Esawi, M.A., Elansary, H.O., El-Shanhorey, N.A., Abdel-Hamid, A.M.E., Ali, H.M., Elshikh, M.S., 2017a. Salicylic acid-regulated antioxidant mechanisms and gene expression enhance rosemary performance under saline conditions. Front. Physiol. 8, 716. El-Esawi, M., Arthaut, L., Jourdan, N., d’Harlingue, A., Martino, C., Ahmad, M., 2017b. Blue-light induced biosynthesis of ROS contributes to the signaling mechanism of Arabidopsis cryptochrome. Sci. Rep. 7, 13875. El-Esawi, M.A., Elkelish, A., Elansary, H.O., Ali, H.M., Elshikh, M., Witczak, I., et al., 2017c. Genetic transformation and hairy root induction enhance the antioxidant potential of Lactuca serriola L. Oxidative Med. Cell. Longevity 2017, Article ID 5604746, 8 pages. El-Esawi, M.A., Mustafa, A., Badr, S., Sammour, R., 2017d. Isozyme analysis of genetic variability and population structure of Lactuca L. germplasm. Biochem. Syst. Ecol. 70, 73 79. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Alayafi, A.A., Witczak, J., Ahmad, M., 2018a. Analysis of genetic variation and enhancement of salt tolerance in French pea (Pisum sativum L.). Int. J. Mol. Sci. 19, 2433.

Plant Life under Changing Environment

832

34. Regulation of genes and transcriptional factors involved in plant responses to abiotic stress

El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Ali, H.M., Alayafi, A.A., Witczak, J., et al., 2018b. Genetic variation and alleviation of salinity stress in barley (Hordeum vulgare L.). Molecules 23, 2488. El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Alamri, S.A., Ali, H.M., Alayafi, A.A., 2018c. Bacillus firmus (SW5) augments salt tolerance in soybean (Glycine max L.) by modulating root system architecture, antioxidant defense systems and stress-responsive genes expression. Plant Physiol. Biochem. 132, 375 384. El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Alzahrani, S.M., Ali, H.M., Alayafi, A.A., et al., 2018d. Serratia liquefaciens KM4 improves salt stress tolerance in maize by regulating redox potential, ion homeostasis, leaf gas exchange and stress-related gene expression. Int. J. Mol. Sci. 19, 3310. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Alayafi, A.A., 2019a. Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stressrelated genes expression. Environ. Exp. Bot. 159, 55 65. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Ahmad, M., 2019b. Overexpression of AtWRKY30 Transcription Factor Enhances Heat and Drought Stress Tolerance in Wheat (Triticum aestivum L.). Genes 10, 163. Espinosa-Ruiz, A., Belles, J.M., Serrana, R., Culianez-Macla, F.A., 1999. Arabidopsis thaliana AtHAL3: a flavoprotein related to salt and osmotic tolerance and plant growth. Plant J. 20, 529 539. Elkelish, A.A., Soliman, M.H., Alhaithloul, H.A., El-Esawi, M.A., 2019. Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiol. Bioch. 137, 144 153. Hasegawa, P.M., Bressan, R.A., Pardo, J.M., 2000a. The dawn of plant salt tolerance genetics. Trends Plant Sci. 5, 317 319. Hasegawa, P.M., Bressan, R.A., Zhu, J.-K., Bohnert, H.J., 2000b. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463 499. Jonak, C., Nakagami, H., Hirt, H., 2004. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol. 136, 3276 3283. Jourdan, N., Martino, C., El-Esawi, M., Witczak, J., Bouchet, P.-E., d’Harlingue, A., et al., 2015. Blue light dependent ROS formation by Arabidopsis Cryptochrome-2 may contribute towards its signaling role. Plant Signal Behav. 10, e1042647. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., Mullineaux, P., 1999. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654 657. Klimczak, L.J., Colline, M.A., Farini, D., Giuliano, G., Walker, J.C., Cashmore, A.R., 1995. Reconstitution of Arabidopsis casein kinase II from recombinant subunits and phosphorylation of transcription factor GBF1. Plant Cell 7, 105 115. Kovalchuk, I., Titov, V., Hohn, B., Kovalchuka, O., 2005. Transcriptome profiling reveals similarities and differences in plant responses to cadmium and lead. Mutat. Res. 570, 149 161. Lee, B.-H., Henderson, D.A., Zhu, J.-K., 2005. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17, 3155 3175. Meagher, R.B., 2000. Phytoremediation of toxic elemental and organic pollutants. Curr. Opin. Plant Biol. 3, 153 162. Morcuende, R., Bari, R., Gibon, Y., Bla¨sing, O., Usadel, B., Czechowski, T., et al., 2007. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ. 30, 85 112. Niyogi, K.K., 1999. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333 359. Osuna, D., Usadel, B., Morcuende, R., Gibon, Y., Bla¨sing, O.E., Ho¨hne, M., et al., 2007. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J. 49, 463 491. Qunimio, C.A., Torrizo, L.B., Setter, T.L., Elllis, M., Grover, A., et al., 2000. Enhancement of submergence tolerance in transgenic rice overproducing pyruvate decarboxylase. J. Plant Physiol. 156, 516 521. Roy, B., Noren, S.K., Mandal, A.B., Basu, A.K., 2011. Genetic engineering for abiotic stress tolerance in agricultural crops. Biotechnology 10, 1 22. Sahi, C., Singh, A., Blumwald, E., Grover, A., 2006. Beyond osmolytes and transporters: novel plant salt-stress tolerance-related genes from transcriptional profiling data. Physiol. Plant. 127, 1 9. Sairam, R.K., Tyagi, A., 2004. Physiological and molecular biology of salinity stress tolerance in plants. Curr. Sci. 86, 407 420.

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Scheible, W.R., Morcuende, R., Czechowski, T., Fritz, C., Osuna, D., Palacios-Rojas, N., et al., 2004. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136, 2483 2499. Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., et al., 2002. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279 292. Va´gu´ifalvi, A., Aprile, A., Miller, A., Dubcovsky, J., Delugu, G., Galiba, G., et al., 2005. The expression of several Cbf genes at the FrA2 locus is linked to frost resistance in wheat. Mol. Genet. Genom. 274, 506 514. Van Assche, F., Clijsters, H., 1990. Effects of metals on enzyme activity in plants. Plant Cell Environ. 13, 195 206. Vinocur, B., Altman, A., 2005. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr. Opin. Biotechnol. 16, 123 132. Vwioko, E., Adinkwu, O., El-Esawi, M.A., 2017. Comparative physiological, biochemical and genetic responses to prolonged waterlogging stress in okra and maize given exogenous ethylene priming. Front. Physiol. 8, 632. Wang, W.X., Barak, T., Vinocur, B., Shoseyov, O., Altman, A., 2003a. Abiotic resistance and chaperones: possible physiological role of SP1, a stable and stabilizing protein from Populus. In: Vasil, I.K. (Ed.), Plant Biotechnology 2000 and Beyond. Kluwer, Dordrecht, pp. 439 443. Wang, W.X., Vinocur, B., Altman, A., 2003b. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1 14. Zhu, J.K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247 273.

Further reading Seki, M., Kamei, A., Yamaguchi-Shinozaki, K., Shinozaki, K., 2003. Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr. Opin. Biotechnol. 14, 194 199.

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C H A P T E R

35 Role of ionomics in plant abiotic stress tolerance Mohamed A. El-Esawi1, Rajeshwar P. Sinha2, Devendra Kumar Chauhan3, Durgesh Kumar Tripathi4 and Jainendra Pathak2,5 1

Botany Department, Faculty of Science, Tanta University, Tanta, Egypt 2Laboratory of Photobiology and Molecular Microbiology, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, India 3D D Pant Interdisciplinary Research Laboratory, Department of Botany, University of Allahabad, Prayagraj, India 4Amity Institute of Organic Agriculture, Amity University Uttar Pradesh, Noida, India 5Department of Botany, Pt. Jawaharlal Nehru College, Banda, India

35.1 Introduction Understanding of the mechanism of life continuity deserves more attention. Hence, it is crucial for understanding the functions and dynamics of the major components of the living cell, including nucleic acids, proteins, and metabolites involved in almost all processes in an organism (Huang and Salt, 2016). Regulation of the uptake and distribution of elements from the soil environment is indispensable for plants. Ionome represents one of the inorganic nutrient components of an organism, which is desirable in small quantities (Salt et al., 2008; Huang and Salt, 2016). Measurement of “ionome” can be done by inductively coupled plasma spectroscopy through an outstanding-throughput pattern of a process called ionomics (Huang and Salt, 2016). Arabidopsis thaliana as a model system has undergone a milestone study to promote the ionomic approach (Lahner et al., 2003; Rea, 2003). Different plant species such as tomato, soybean, barley, rice, maize, Lotus japonicus, and others have also been introduced into the ionomic approach (Watanabe et al., 2007; Chen et al., 2009a,b; Sa´nchez-Rodriguez et al., 2010; Parent et al., 2013; Wu et al., 2013; Ziegler et al., 2013; Baxter et al., 2014; Gu et al., 2015; Pinson et al., 2015; Huang and Salt, 2016). The ionome assists in performing several functions in the plants such as censoring the functions

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of the plant genome. Furthermore, several genetic mapping approaches have participated significantly in the prosperity of ionomics including deletion mapping, bulk segregant analysis (BSA) based on DNA microarray as well as sequential mapping (Baxter et al., 2009; Chao et al., 2011; Kamiya et al., 2015; Huang and Salt, 2016). Abiotic stress adversely affects plants growth and development (El-Esawi and Alayafi, 2019a,b; Vwioko et al., 2017; El-Esawi et al., 2017a, 2018a,b,c,d, 2019a,b; Elkelish et al., 2019; Elansary et al., 2017), resulting in the excessive formation of harmful reactive oxygen species (ROS) (El-Esawi et al., 2015, 2017b). In addition to the important application of genetic and metabolomic approaches in improving plant performance, development and stress tolerance (Elansary et al., 2018; El-Esawi and Sammour, 2014; El-Esawi 2016a,b,c, 2017a,b; El-Esawi et al., 2016a,b, 2017c,d), ionomics approaches have also exhibited pivotal roles in plant abiotic stress responses. The present chapter emphasizes on the ionomics approach employed against various abiotic stress factors that affect growth and performance of plants.

35.2 Forward genetics and ionomic gene identification Lahner et al. (2003) have studied a number of mutant leaves with altered ionomic profiles. The results of screening 4747 M2 fast neutron (FN) mutant revealed that altered accumulation of multiple or single elements were observed in around 338 mutants (Huang and Salt, 2016). Of the FN mutants, 44 are clustered in a hierarchical shape by using the leaf ionome, which in turn acts as a phenotype for such clustering of mutants. Hence, these findings reveal that the clustering of mutants does not depend on the soil batch or plant cultivation tray (Huang and Salt, 2016). Lahner et al. (2003) have carried out an experiment using the forward genetic screen to develop a first ionomic mutant called enhanced suberin1-1 (esb1-1). They also named it 145:01. Such mutant has several consequences. One of them is the perturbation of the lignin deposition needed for developing Casparian strip
like structures (Huang and Salt, 2016). This will further result in ectopic deposition of both suberin and lignin at the endodermis (Halpin, 2013; Hosmani et al., 2013; Huang and Salt, 2016). The phenotype of esb1 mutant is a multitasking element that causes minimal accumulation of Ca, Mn, and Zn (Huang and Salt, 2016). Meanwhile, it efficiently helps in the accumulation of Na, K, S, Se, As, and Mo at higher levels in plant leaves (Huang and Salt, 2016). The improved myb36-1 mutant is the second multitasking ionomic mutant, which was isolated by Lahner et al. (2003) who called it as 112:50 (Franke, 2015; Kamiya et al., 2015). Kamiya et al. (2015) have also reported the importance of the MYB36, a transcription factor in mediating expression of ESB1, peroxidase 64 (PER64), and Casparian strip domain proteins, which are necessary in developing Casparian strips (Huang and Salt, 2016). However, mutations in MYB36 have an adverse effect on the plant leaves such as absence of ectopic endodermal suberin, lignin, and Casparian strips, reducing the accumulation of Ca, Mn, and Fe, while enhancing the concentration of Mg, Na, and Zn in the leaves (Kamiya et al., 2015; Huang and Salt, 2016). Moreover, developing Casparian strips in the cortex and the epidermis is the function of MYB36 ectopic expression (Huang and Salt, 2016). There is an urgent need to study the possible role of Casparian strips formation in the ionome efficiency despite the incomplete formation of such Casparian strips. The tsc10a-1 mutant is another example exhibiting an ionomic

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phenotype (Huang and Salt, 2016). It was discovered by Chao et al. (2011) who named it 71:13 and is characterized with improved suberin deposition and altered sphingolipid induction in the plant root. Tsc10a-1 displays a multitasking phenotype, which enhances the accumulation of Na, K, and Rb and reduces the levels of Ca, Mg, Fe, and Mo in the plant leaves (Huang and Salt, 2016). Several findings revealed the importance of Casparian strip in the adjustment of the ionome of leaf. Hence, it would be interesting to highlight whether the formation of Casparian strip
like structures is based on the TSC10A (Huang and Salt, 2016). Pfister et al. (2014) isolated the schengen3 (sgn3) mutant from a forward genetic screen. This mutant exhibited a deficiency in Casparian strip formation (Huang and Salt, 2016). Although the mutants esb1 and myb36, along with the casp1 and casp3 double mutant (Hosmani et al., 2013), displayed functional Casparian strip
like structures, however, sgn3 shows deficiencies in the formation of Casparian strips while exhibiting several ionomic changes by increasing Mg levels with lowering K levels in leaves (Huang and Salt, 2016). A mutant named 117:20 showed fluctuations in the ionomic properties, which was isolated by Lahner et al. (2003), showed lower K and higher Mg in leaves. The relation between endodermal diffusion barriers as a natural biological pathway and similar ionomic phenotypes produced reveals that clustering of ionomic-related mutants in hierarchical shape could shed light on identifying modern mutants within the same biological system (Huang and Salt, 2016). This is derived from the certainty that different myb36, esb1, and tsc10a alleles that grow in similar experimental blocks (such as plant cultivation trays and soil batches) are found to exhibit ionomic clustering together (Huang and Salt, 2016). Hence, the trend will be toward the possibility of cloning obscure mutants that are able to cluster ionomically with those disrupted in such as Casparian strip development. Casparian strips are thought to be the major factors for ionome conservation in plants (Huang and Salt, 2016). This raises the intriguing possibility for the role of the Casparian strip
developing endodermis in regulating the selective diffusion of water and nutritional minerals into the plant roots followed by their translocation to the shoot system (Geldner, 2013). Kamiya et al. (2015) highlighted the endodermal function in preventing the direct movement of mineral ions from cortex to the stele and vice versa (Huang and Salt, 2016). Disruption of Casparian strip formation resulted in the disordered influx of ions from and to the cortex (diffusion of ions occurs from cortex to stele when ions are at high level of concentration in cortex and lower level in the stele and vice versa) (Huang and Salt, 2016). This derives the conclusion that the movement of ions across the endodermis is linked to the ionomic changes detected in Casparian strip
like mutants. Deficiency in the formation of Casparian strip
like structures is found to be related to the absence of SGN3 function resulted in the redistribution of both elements K and Mg in the endodermis with higher level of K concentration in the stele rather than the cortex in conjunction with a decreased Mg concentration in the stele compared with the cortex (Huang and Salt, 2016). Compensative ectopic endodermal suberin and lignin of esb1 and myb36 mutants along with the deficiency in Casparian strip formation are reported to be the major consequences of the complicated ionomic changes of both mutants (Huang and Salt, 2016). Ectopically deposited lignin and suberin not only influence the apoplastic but also the transmembranal ion transport from the cortex to the stele and vice versa. Barberon et al. (2016) have reported that the transportation of suberin depends on the status of mineral nutrients of

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the cell. Lahner et al. (2003) have identified a variety of ionomic mutants with deficiencies in Casparian strip production, for example, the nakr1-1 mutant, which causes disturbance of Na and K uptake by root (Huang and Salt, 2016). Meanwhile, Na and K are translocated to the phloem by NaKR1 (Tian et al., 2010), which is also responsible for encoding a metalbinding protein. Several minerals including K, Na, and Rb are assimilated by nakr1-1 mutant. However, the molecular mechanism of such mutant is unclear (Huang and Salt, 2016). There is no relevance between reduced K accumulation and promoted salicylic acid and jasmonic acid, which play the role in adaptation of cpr5 mutants to pathogen stress (Borghi et al., 2011). Meanwhile, in cpr5 shoots, cyclic nucleotide-gated channel levels increased in compatibility with reduced levels of high-affinity potassium transporter (HAK5) in roots could participate effectively in such pattern (Borghi et al., 2011; Huang and Salt, 2016). In addition, the absence of ionomic phenotypes from an outcross mapping F2 population was the major cause behind the loss-of-function bulk segregant mapping of F2 progeny (Huang and Salt, 2016). This afterward supports the role of parental natural variation in inhibition of the mutant phenotype. Abe et al. (2012) have utilized the background mutations as markers for mapping of mutagenized lines (Huang and Salt, 2016). This will subsequently lead to alleviated mutant phenotype breakthrough in an outcrossed F2 progeny (Huang and Salt, 2016).

35.2.1 Natural resources and ionomic alleles identification Several techniques are utilized to detect genes causing differences in ionomic phenotypes such as quantitative trait loci (QTL) mapping or conventional linkage mapping. Such detection is promoted through introducing biparental crosses between accessions from the phenotypic extremes (Huang and Salt, 2016). Rus et al. (2006) have displayed an encoding gene for Na transporter, which is called HKT1;1. The accessions Tsu-1 and Ts-1 of A. thaliana showed elevated concentration of Na1 in leaves because of this gene (Huang and Salt, 2016). Na was found to be accumulated at high rates in the accession leaves under limited HKT1;1 expression usually through a deletion in its promoter (Huang and Salt, 2016). The mechanism by which genetic variations in HKT1;1 coding region function remains unknown, whereas a polymorphism involved in FPN2 coding regions is likely to be responsible for genetic changes in Ts-1 and Se-0 accessions of Co leaves as well as changes in Fe homeostasis (Morrissey et al., 2009; Huang and Salt, 2016). Moreover, Chao et al. (2014a,b) have identified Adenosine 50-Phosphosulfate Reductase2 (APR2) gene in F2 progeny using DNA microarray-based BSA technique and revealed that such gene is causal for Se and S variation in Hod A. thaliana accession (Huang and Salt, 2016). There is a connection between the enzymatic rate and the variation in APR2 amino acid sequence. While selenate and sulfate variation is lowered by such genetic variation as it enhances Se and S accumulation at higher levels (Huang and Salt, 2016). Moreover, of 855 APR2 alleles across A. thaliana accessions, 11 haplotypes were found to include variations in amino acid sequences of the protein. Despite the contribution of mapping technique in identifying ionomic QTLs (Huang and Salt, 2016), occasionally, it fails to detect the genetic variation within several phenotyped accessions. For example, the F2 mapping model fails in identification of the genetic variation for K assimilation in the Wa-1 accession. Subsequently,

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Chao et al. (2013) have reported that the ploidy of the root was the major contributor in the variation of constantly increased K level in Wa-1 cytotype in leaves. In addition, recombinant inbred lines (RILs) are another technique used for detecting the ionomic QTLs (Huang and Salt, 2016). It aims to develop imperishable homozygous phenotypes from crossing two parental strains followed by self-mating among the mature generations (Huang and Salt, 2016). For example, Loudet et al. (2007) have identified APR2 gene for ionomic analysis for QTLs from the generation of Bay-0 3 Shahdara RIL transcripts. Such gene is causal for regulating accumulated sulfate variation in leaves. In addition, ATP sulfurylase 1 is another gene regulating the accumulation of sulfate in leaf using RIL technique (Koprivova et al., 2013). It is well known that changes in APR2 coding regions will affect S phenotypes (Loudet et al., 2007; Chao et al., 2014b; Huang and Salt, 2016). Mapping using sequencing of F2 population along with RILs analysis could also serve as a promising approach (Baxter et al., 2008; Huang and Salt, 2016). Several studies have also developed sequenced phenotypes of Col-0 3 Ler-0 F2 F2 population using DNA microarray-based BSA approach to detect the specific locus that reduces the Mo concentration in Ler-0 accession then they analyzed the RILs produced from the recombinated break points of Col-0 3 Ler-0 RIL population to select the target causal locus (Huang and Salt, 2016). The results provide information about the role displayed by Mo transporter 1 (MOT1) variance in natural variation of Mo in Ler-0 (Huang and Salt, 2016). The deletion of 53-bp in the promoter represents the practical polymorphism in MOT1 in Ler-0 (Tomatsu et al., 2007; Baxter et al., 2008; Huang and Salt, 2016). However, a survey conducted on the MOT1 promoter of 283 accessions displayed only six polymorphisms showing deficiency in encoding the phenotypes (Forsberg et al., 2015; Huang and Salt, 2016). Interestingly, only two polymorphisms were strongly affected by Mo variation in the 340 accessions (Huang and Salt, 2016).

35.3 Effect of heavy metal on plants Ionomics refers to the investigation of the cellular ionome, which encompasses the quantification of composition of various elements in tissues as well as organisms along with their alterations with respect to physiological processes or stresses (biotic/abiotic) (Salt et al., 2008). “Heavy metals (HMs)” are metallic elements having relatively high density and are toxic to plants/organisms even at very low levels (Lenntech Water Treatment and Air Purification, 2004). HMs, such as Fe, Zn, and Cu, are essential nutrients for animals and plants (Wintz et al., 2002). HMs alter metabolic and physiological processes of plants causing damage to them. As mentioned earlier in plants HMs, such as Zn, Cu, Fe, Mo, Mn, Co, and Ni, serve as essential micronutrients, and there is a variation in availability of HMs in medium (Reeves and Baker, 2000), which when uptaken in excess amount than their requirement become toxic to plants (Blaylock and Huang, 2000; Monni et al., 2000). Both excess availability and deficiency of HMs are harmful to the plants as some of these HMs are essential micronutrient of plants. Higher concentrations of elements such as Hg, Cd, and As become toxic to the cellular metabolic/physiological activities of plants (Foy, 1978).

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35.3.1 Mechanism of heavy metal toxicity in plants Molecular oxygen when accepts electrons from other molecules results in the production of oxygen-free radicals and reduction of O2 to hydrogen peroxide (H2O2) or superoxide (O2 2 ) occurs through many intracellular reactions. As such these molecules are inert/ not much reactive but they have tendency to form hydroxyl radicals (2OH), and these radicals are the most damaging radicals in biological systems causing oxidative stress in plants (Halliwell and Cutteridge, 1990). Thermodynamically formation of superoxide radical through the reduction (one-electron) of O2 is unfavorable (Illan et al., 1976), but this can be facilitated by reacting with other paramagnetic center. Unpaired electrons, which occur frequently in transition metals (M) such as Cu and Fe, serve as suitable catalysts for the reduction of O2 as shown in the following reaction: Mn 1 O2 -Mn11 1 O2 2 In aqueous mediums, at neutral pH, the formation of H2O2 from O2 2 occurs, which decomposes to produce OH, involving Fe or Cu (M) as shown in the reaction: n Mn11 1 O2 2 -M 1 O2

Mn 1 H2 O2 -Mn11 1 OH2 1 OH ðHaber-Weiss reactionÞ Overall the previous reaction can be written as O2 1 H2 O2 -O2 1 OH2 1 OH “Fenton reaction” refers to Haber
Weiss reactions involving Fe as catalyst. Through Haber
Weiss reactions, metal ions also play a crucial part in the oxidative modifications of proteins and free amino acids (Stadtman, 1993).

35.4 Toxicity of heavy metals in plants In polluted soils, concentration of Zn varies from 150 to 300 mg/kg (Warne et al., 2008). The toxicity of Cd and Zn was evidenced as decrement in metabolism, development and growth of plants, and induction/initiation of oxidative stress/damage in plants such as Phaseolus vulgaris and Brassica juncea (Cakmak and Marshner, 1993; Prasad and Hagmeyer, 1999). In plants, growth of both shoot and root was limited by Zn toxicity (Ebbs and Kochian, 1997; Fontes and Cox, 1998). Plants growing in soils having high Cd levels show symptoms of damage/injury such as growth inhibition, chlorosis, root tips browning, and leaf rolls, which finally lead to death of plant (Mohanpuria et al., 2007; Guo et al., 2008). Cd interferes with several metabolic processes of plants such as uptake of nutrients, their transportation, and utilization of mineral elements, namely, Mg, Ca, K, and P, and water (Das et al., 1997). Enhanced levels of Cd also inhibits the nitrate reductase activity in shoots of plants thereby reduces uptake and transportation of nitrate from their roots to shoots (Hernandez et al., 1996). Ca21 reduces Cd21 uptake and toxicity (Hinkle et al., 1987; Karez et al., 1990). Excess of Cu in soil causes injury to plants as it is cytotoxic and induces stress in plants leading to retarded plant growth and chlorosis of leaves

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(Lewis et al., 2001). Before eventually becoming necrotic, leaves become wilted in acute Cu toxicity (Foy et al., 1995). Coating of seeds by organic mercurials for preventing seedborne fungal diseases is the most important source of agricultural soil contamination (Patra and Sharma, 2000). Physiological disorders and injuries can be induced by toxic levels of Hg21 in plants (Zhou et al., 2007). Various physiological, morphological, and biochemical processes get influenced by Pb in plants (Pourrut et al., 2011). In plants, Pb mostly penetrates through the roots barring certain areas where significant atmospheric fallout occurs (Uzu et al., 2009, 2010; Schreck et al., 2012). In plants, even small amount of Pb which penetrates into the symplast can result in several deformities (Singh et al., 2016; Seregin and Ivanov, 2001; Pourrut et al., 2011).

35.5 Ionomics of heavy metals Mineral elements including N, P, K, Ca, Mg, Fe, Cu, Mn, Mo, Co, and Zn have been found to be involved in alleviating damage induced by HMs to the plants. Transporters located in the plasma membrane or tonoplasts are actively involved in maintenance of cellular metal homeostasis under permissible limit in order to avoid mineral/trace elements
induced toxicity. These elements/ions are chelated through low-molecular-weight compounds/chelators and are excluded to extracellular spaces or sequestrated in vacuoles by these transporters (Singh et al., 2016). These cellular transporters belong to any of the categories that are discussed in the following section.

35.5.1 P1B-ATPases/heavy metal ATPases P1B-ATPases are found in prokaryotes as well as eukaryotes ranging from yeasts, insect, mammals to higher plants. These ATPases play a crucial role in the detoxification, transportation, and compartmentalization of HMs as they translocate HMs from cytoplasm to the plasma membrane and into the vacuole of the plant cell utilizing the energy produced from ATP hydrolysis (Williams et al., 2000; Grennan, 2009). Zn and Cd are exported through HMA2, HMA3, and HMA4. HMA4 protein has been found to be involved in Zn transport from roots to shoots, nutrition, and Cd efflux thereby protects the plants as well (Mills et al., 2005). Although in Arabidopsis for maintenance of Zn homeostasis HMA2 and HMA4 were found to be important, hma2 and hma4 (the double mutants of HMA2 and HMA4) were found to be more sensitive to high levels of Cd indicating their possible role in Cd detoxification (Hussain et al., 2004). In the same manner, in Arabidopsis this loss of functioning in HMA2 and HMA4 enhanced their sensitivity to Cd under phytochelatins deficient, cad1-3 as well as CAD1 backgrounds (Wong and Cobbett, 2009). In A. thaliana for variation in Cd accumulation/uptake, HMA3 was found to be solely responsible as observed in its 349 wild varieties, from techniques such as transgenic complementation, linkage mapping as well as genome-wide association mapping. Plant varieties with higher levels of Cd accumulation indicated reduced functioning of HMA3 (Chao et al., 2012). In the same way, expression of C-type ATP-binding cassette transporter (OsABCC) family was studied, and its role in reducing/nullifying the accumulation of As Oryza sativa grains

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was studied by Song et al. (2014). Under higher level of As, higher expression of these transporters was observed (Song et al., 2014).

35.5.2 Natural resistance-associated macrophage protein transporters Plasma membrane of apical cells of root contains natural resistance-associated macrophage protein (NRAMP), the integral membrane protein family, which is highly conserved in several species of plants (Simo˜es et al., 2012). NRAMPs have role in H1-coupled active transport of different HMs (Cd21, Zn21, Fe21, Co21, Mn21, Ni21, Cu21, and Pb21) in phylogenetically different organisms, for example, microorganisms (bacteria and fungi), animals, and plants (Hall and Williams, 2003; Cailliatte et al., 2009). Specific transport of Al is performed by this transporter gene (Xia et al., 2010). Nramp5 transporter specifically transports Cd and Mn (Sasaki et al., 2012).

35.5.3 Cation diffusion facilitators/Metal tolerance proteins Nies and Silver (1995) first of all reported cation diffusion facilitators (CDFs) family in taxonomically different organisms including fungi, bacteria, plants, and animals. Transporters of this family maintain HMs homeostasis of cell having prime selectivity toward Zn21, Fe21, and Mn21 (Podar et al., 2012). CDF transporters cause efflux of HMs from cytoplasm either into the cell organelles or to extracellular space (Haney et al., 2005; Ricachenevsky et al., 2013). In A. thaliana and O. sativa, 12 and 10 MTP genes have been recognized respectively (Gustin et al., 2011).

35.5.4 ZRT, IRT-like proteins transporters ZRT, IRT-like protein (ZIP) family transporters transport HMs from organelles lumen or from extracellular space into the cytoplasm. Fifteen genes of the ZIP family are reported in Arabidopsis, namely, ZIP1
12 and IRT1
3 (Milner et al., 2013). In plants the role of AtIRT1 in regulating the homeostasis of Fe and Zn was reported. In plants, transporters of Si (Lsi1; low silicon 1, influx transporter: Lsi2; low silicon 2, efflux transporter) regulate uptake of As (arsenite) (Eide et al., 1996; Ma et al., 2008; Lin et al., 2009; Vert et al., 2009). Another transporter, for example, arsenate reductase (ACR), has also been reported, which was characterized in Saccharomyces cerevisiae and serves as model system for As resistance. In S. cerevisiae arsenite (AsIII) resistance was found to be conferred by 4.2-kb region. Three ACR genes have been reported, namely, ACR1-3 (Bobrowicz et al., 1997). ACR2 and ACR3 were found to be regulated by ACR1 through transcriptional factor, and it was also found that yeast conferred arsenate and arsenite hypersensitivities on any loss in ACR1 function (Bobrowicz et al., 1997; Ghosh et al., 1999). Arsenate reductase is represented by ACR2, which shows homology with yeast ASCR2 (ScACR2) (Landrieu et al., 2004a,b). Similarly, in Pteris vittata transporter PvACR2 was reported, and from O. sativa transporters OsACR2.1 and OsACR2.3 were reported (Ellis et al., 2006; Duan et al., 2007). In A. thaliana, ACR2 (CDC25) plays a role in As metabolism. However, at present role of new ACR, HAC1, or ATQ1 was reported in A. thaliana

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35.7 Role of osmolytes in plant protection

FIGURE 35.1

Toxic metals (As, Cd, Pb, Cu etc.) Receptors Alterations in electron transport chain I

II

Q

III

IV

Mitochondria

Signal transduction such as cAMP, and pH

SA, BRs, GAs

Generalized mechanism of heavy metal stress response in plants. Source: Modified from Singh, R. P., Tripathi R.D., Sinha, S.K., Maheshwari, R., Srivastava, H.S., 1997. Response of higher plants to lead contaminated environment. Chemosphere 34, 2467
2493. https://doi.org/10.1016/S0045-6535(97) 00087-8.

Transporter proteins Hame oxygenase-1 BES1, BZR1, GA-GIDI-DELLA Chloroplast

Antioxidants

Defense genes, TFs, HSP, MTs

Excess ROS

Oxidative damage

Metal tolerance

nucleus

(Chao et al., 2014a,b; Sa´nchez-Bermejo et al., 2014). In A. thaliana, loss of HAC1 function caused decreased As accumulation in roots resulting in decreased As efflux to external medium (Chao et al., 2014a,b). In O. sativa, another transporter, OsABCC1, was found to be localized in phloem cells and plays an important role in As sequestration to cell’s vacuole (Song et al., 2014). Generalized mechanism of HMs stress response in plants has been depicted in Fig. 35.1.

35.6 Salt stress and plants Salinity has affected about 6% of the total agricultural land worldwide (Munns and Tester, 2008). During salt stress, all major processes of plants including protein synthesis, photosynthesis, and lipid metabolism are affected and thereby resulting in increase or decrease in concentrations of various metabolites taking part in numerous metabolic processes in the cell. Polyols (sorbitol/mannitol), sugars (sucrose, trehalose, and fructan), dimethylsulfonium [glycine betaine (GB), dimethylsulfopropionate], and amino acids (proline and ecotine) are certain plant metabolites involved during biotic/abiotic stress responses acting as osmoprotectant and osmolytes as an adaptive strategy for protecting plants in conditions of high salt concentrations and other stresses (Shulaev et al., 2008).

35.7 Role of osmolytes in plant protection Osmotic balance and structure of cell is maintained by osmolytes present within the cell, which mediates influx of water continuously inside the cell (Hasegawa et al., 2000).

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On exposure to high salt concentrations, there is significant change in the cell’s amino acid concentrations as arginine, cysteine, and methionine content decreases, whereas concentration of proline increases during salinity stress (El-Shintinawy and El-Shourbagy, 2001). Intracellular proline aids in providing tolerance toward salt stress as well as serves as an organic reservoir of nitrogen during recovery from stress. GB is a cellular osmolyte, which is nontoxic and plays an important role in stress mitigation/tolerance along with several other functions such as protecting the cells by osmotic adjustments, protects the photosynthetic apparatus, stabilizes proteins, and reduces ROS generation (Ahmad et al., 2013). In the plants that are exposed to salinity stress, when GB is applied as a foliar spray, photosynthetic rate and growth of plants are enhanced, and pigment stabilization was also reported (Ahmad et al., 2013). Accumulation of carbohydrates, that is, sugars and starch (glucose, sucrose, fructose, and fructans), was observed during salt stress, which acts as osmoprotectants for osmotic adjustment along with playing role in carbon storage and radical scavenging (Parida et al., 2002). Trehalose was found to be playing osmoprotective part during physiological responses to salinity stress (Ahmad et al., 2013). In plants that are under salt stress, inositol accumulation serves as free radical scavenger (Smirnoff and Cumbes, 1989; Gong et al., 2005; Gagneul et al., 2007). In rice, tobacco, and Arabidopsis, salt tolerance was enhanced by the overproduction of diamine putrescine, triamine spermidine, and tetra-amine spermine (Roy and Wu, 2002). Regulation of protein folding assembly, Calvin cycle, and triamine spermidine
mediated inhibition of protein proteolysis also contribute to tolerance of plants during salt stress (Li et al., 2013). In several plant species, toxic effects of salinity were found to be lessened by the exogenous application of antioxidants, which is also promoted recovery of plants from the stressed conditions (Agarwal and Shaheen, 2007; Munir and Aftab, 2011). Under salt stress, higher levels of organic acids help in improving plant growth. Enhanced concentrations of organic acids result in increased production of ATP, NADH, and FADH2, and this might be due to increased C flow from glycolysis via tricarboxylic acid (TCA) cycle. In response to salinity stress, osmotin is one of the most extensive proteins accumulated in the plant cells. In plants the vacuolar-type H1-ATPase plays a pivotal role in salinity stress tolerance with enhanced expression and enzymatic activity (Golldack and Dietz, 2001). Ca21, which acts as signal of salt stress, is sensed by salt overly sensitive (SOS) proteins and switching on the pathway for K1/Na1 discrimination and Na1 export. In plants during salt stress, for maintenance of ion homeostasis and stress-signaling pathway, the SOS response serves as crucial regulator (Hasegawa et al., 2000).

35.7.1 Role of late-embryogenesis-abundant- type proteins in salt stress Genes such as early responsive/responsive to dehydration, responsive to abscisic acid (ABA), and cold inducible/regulated (KIN/COR) genes, code for “late-embryogenesisabundant (LEA)” proteins are induced during osmotic stresses in several plant species (Shinozaki and Yamaguchi-Shinozaki, 2000). CRT/DRE elements regulate the expression of genes under the conditions of dehydration (drought, cold, and salt stress), which are located on the promoter region of LEA-like genes, whereas during abiotic stresses MYC/ MRB-mitochondrial RNA-binding complex and ABA-responsive element (AREB) elements

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control genes expression in response to ABA (Thomashow, 1999; Shinozaki and Yamaguchi-Shinozaki, 2000). Regulation of LEA-type genes expression under the condition of osmotic stress occurs by both ABA-independent and -dependent signaling pathways. During osmotic stress, in the case of ABA-dependent expression, regulation occurs through the transcription factors such as MYB/MYC type and basic leucine zipper for recognition MYB/MYC and ABRE recognition sequences, respectively (Uno et al., 2000; Abe et al., 2003). Regulation of LEA-type genes via ABA-independent pathway involves transcription factors for the activation of CRT/DRE cis-elements of LEA-type genes. High soil salinity results in ion toxicity, water deficit, rapid decrement of growth rate, nutrient deficiency and causes several metabolic changes resulting in molecular damage of the cell, thereby affecting the overall growth and development of plants that are sensitive to salt (Hasegawa et al., 2000; Flowers, 2004; Wang et al., 2007; Sobhanian et al., 2011). In high salt conditions, halophytes adopt the following survival strategies (Mahajan and Tuteja, 2005; Gagneul et al., 2007; Sanchez et al., 2008; Stepien and Johnson, 2009; Shabala and Mackay, 2011; Slama et al., 2015; Uzilday et al., 2015): 1. 2. 3. 4. 5.

Accumulation or selective exclusion of ions Controlled uptake of ions by roots (especially K1) and its transportation to leaves Cellular/Whole-plant level compartmentalization of ions Production of compatible solutes and osmoprotectants Alterations in photosynthetic pathway

For counteracting the harmful effects of excess salinity in their cells, the salt-loving plants, halophytes withstand the high concentration of salt by the presence of saltresponsive genes/proteins in their cells (Askari et al., 2006; Yu et al., 2011). In the postgenomic era, proteomics and metabolomics have emerged as important “-omic” techniques, which can reflect the alterations taking place in plants on exposure to salt stress (Fernandez-Garcia et al., 2011; Zhang et al., 2013). Adaptations during salt stress include enhanced amount and activity of ion transporters (SOS1) present in plasma membrane for exclusion of salt ions, H1 ATPase, tonoplast ion transporters NHX and folate-binding protein (FBP) aldolase for compartmentalization of salt ions (intracellular) and prevention of Na1 back-leak into cytosol by blocking Na1 permeable FV and SV channels of tonoplast (Tada and Kashimura, 2009; Wakeel et al., 2011; Bonales-Alatorre et al., 2013; Yuan et al., 2015).

35.8 Ionomics of salt stress For counteracting the high salinity-induced toxicity, plants acclimatize through changing ion uptake and their transport or partitioning (Sanchez et al., 2008). For functioning of normal cells in plants, ratio of K1/Na1 should be high. Poor retention of K1 results in its deficiency in the cytosol at higher Na1 concentration as membrane depolarization induced by Na1 causes efflux of K1 via KOR channels, which gets activated through depolarization (Shabala and Mackay, 2011; Bose et al., 2014). Entry of Na1 into the cytosol occurs through selective/nonselective transporters as well as via cation channels in the saline environment (Sanchez et al., 2011). During salt stress, Ca plays a significant role in

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signaling as Na1 influx is directly altered by extracellular Ca1 and followed by the maintenance of K1 and Na1 homeostasis by SOS pathway (Mahajan and Tuteja, 2005). Membrane transporters maintain ion homeostasis such as SOS transporters (SOS1), H1ATPase, Na1/H1 exchanger (NHX1), and high-affinity K1 transporters (Shi et al., 2002; Maathuis, 2006; Sanadhya et al., 2015). For expelling Na1 outside the cell, SOS1
3 along with a Ca21 sensor play an important role in SOS1 pathway (Khan, 2011). Through the Ca21 signals, SOS3 perceives the extracellular salt stress signals. SOS2 (a serine/threonine protein kinase) in turn is activated by the SOS3. Phosphorylation of SOS1 transporter occurs by the activated SOS2, the plasma membrane Na1/H1 antiporter, for transporting Na1 outside the cytosol.

35.8.1 HKT-type Na1 transporters HKT-type Na1 transporters are responsible for keeping Na1 concentrations of cytosol low. In soil, HKT1 has role in loading of Na1 ions into the plant’s vascular tissue and cation uptake. This results in accumulation of Na1 ions in leaves of Mesembryanthemum crystallinum during hypersalinity conditions (Su et al., 2003).

35.8.2 V-type H1 ATPases V-ATPase (member of H1-ATPase) is a complex made up of multiheteromeric subunits consisting of at least 11 different subunits present in base
stalk
head-like order and is located on the tonoplast of the cell (Shabala et al., 2014). By transporting protons across the tonoplast, V-type H1-ATPase forms proton gradient that helps in active influx of Na1 inside the vacuole and thereby decreasing the toxic concentrations of Na1 in the cell’s cytoplasm. Hence, accumulation of Na1 inside the vacuole of the cell serves as an important mechanism for maintenance of cell osmosis in plants by balancing Na1 concentration in cytoplasm (Du et al., 2010). Salt glands or bladders (specialized epidermal cells) have been developed by several halophytes for eliminating excess salts from metabolically active tissue (Agarie et al., 2007; Flowers and Colmer, 2008; Shabala et al., 2014).

35.9 Effect of osmotic stress on plants Osmotic pressure is increased in the cytosol during salt and drought stresses due to deficiency (drought) of water or by excessive uptake of the salts resulting in salinity stress. To tolerate/exclude excessive salts within/from the cells, different strategies are developed by salt-tolerant species (Parida and Das, 2005). Growth of plant and its survival, distribution, and yield are effected by availability of water to plants. Osmotic stress effects the growth and development of plants. It leads to induction of oxidative secondary stress that increases in ascorbate breakdown products and homoglutathione as well. Tolerant species adjusts to osmotic stress by the following two ways (Munns, 2002): 1. Sequestration of excessive salts into the vacuole of the plant cells 2. Synthesis of osmoprotactant compounds inside the cells

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On exposure to osmotic stress, novel proteins are synthesized and accumulated by plants, and such polypeptides can be identified either through one- and two-dimensional gel electrophoresis (Hurkman and Tanaka, 1988; Hurkman et al., 1988). Most of the osmotic stress
regulated (OR) genes encode LEA proteins that get activated during osmotic stress occurring due to conditions of drought, high salt concentrations, or low temperatures (Baker et al., 1988; Dure et al., 1989). It was found that most LEA genes respond to ABA (Skriver and Mundy, 1990). During osmotic stress in plants, for preventing loss of water and regaining turgidity, cells accumulate ions/solutes mainly Na1, K1, and C12 and organic compounds such as betaines and proline (Rhodes, 1987). Induction of ATPase genes of plasma membrane and tonoplast occurs during high salt conditions (Surowy and Boyer, 1991; Niu et al., 1993a,b; Binzel, 1995). Accumulation of elongation factor 1-alpha, which is essential component of protein synthesis, is enhanced significantly in salt-adapted fungal and tobacco cells (Zhu et al., 1994). Induction of heat shock proteins (HSPs) during osmotic stress was found in rice cells as evidenced by accumulation of HSP70 gene as osmotic stress adaptation (Borkird et al., 1991; Vierling, 1991). HSPs prevent protein denaturation and assist in protein folding hence function as molecular chaperones (Zhu et al., 1993). During high salt, dehydration, and cold stress in addition to osmotic stress induction of the osmotin gene was found in viral and fungal pathogens (Kononowicz et al., 1992; LaRosa et al., 1989). ABA acts as important player in regulating and responding to low water availability, during several developmental processes and other environmental cues (Finkelstein et al., 2002; Yamaguchi-Shinozaki and Shinozaki, 2006). Endogenous levels of ABA increases in plants because of cellular dehydration during maturation of seeds and osmotic stress at the time of postgermination growth (Fujita et al., 2011). It also induces several drought-responsive genes (Fujita et al., 2011). Majority of genes which are induced by ABA, their promoter regions contain a well-conserved G-box-like cis-acting elements and are designated as ABREs (PyACGTGG/TC) (Mundy et al., 1990; Busk and Page`s, 1998; Hattori et al., 2002; Zhang et al., 2005; Go´mez-Porras et al., 2007; Maruyama et al., 2012). Fig. 35.2 depicts the generalized mechanism of plant’s response under the conditions of osmotic stress.

35.10 Ionomics of osmotic stress In soil and pore water if Na concentration increases, it may result in decreased activities of nutrient ion and causes an increase in Na/K ratio, whereas deficiency of Mg and Fe may be induced due to high Zn concentrations because of similarity in the ionic radius of Fe21
Zn21 and Mg21
Zn21 (Boardman and McGuire, 1990; Gratten and Grieve, 1999; Sagardoy et al., 2010). Deficiency of Mg12 stimulates H2O22 and O2 scavenging systems (Cakmak and Marschner, 1992a). In the absence of Mg21, plants become highly resistant to paraquat injury induced by light and mediated through superoxides (Cakmak and Marschner, 1992b). Salt stress induces ROS generation resulting from leakage of electrons toward oxygen, produced due to defective electron flow owing to alterations in ionic interactions of membrane (Koyro, 1997; Borsani et al., 2001; Slesak et al., 2002). Enzymatic activity of NADPH oxidase can result in the production of ROS (Kawano et al., 2001). Rapid enhancement in accumulation and biosynthesis of phosphatidylinositol (1,4,5) P3 and (4,5)

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Drought stress

Salt stress

Osmotic stress Cold stress

Signal transduction pathway protein kinases, IP3, Ca2+, MAPK, etc.

Transcription factor

Cytoplasmic protein

OSRF OSRE

mRNA OSRG Transcriptional processing

mRNA

Cytoplasmic protein synthesis

OSP Biochemical responses

Cellular response

Osmotic stress response and tolerance

FIGURE 35.2 Generalized mechanism of osmotic stress response in plants. OSP, Osmotic stress proteins; OSRE, Osmotic stress responsive elements; OSRF, osmotic stress responsive factors; OSRG, osmotic stress responsive genes. Source: Modified from Upadhyaya, H., Sahoo, L., Panda, S.K., 2013. Molecular physiology of osmotic stress in plants. In: Rout, G.R., Das, A.B. (Eds.), Molecular Stress Physiology of Plants. Springer, India, pp. 179
192. Available from: https://doi.org/10.1007/978-81-322-0807-5_7.

P2 as an early molecular response is observed during hyperionic and hyperosmotic stress conditions (Pical et al., 1999; DeWald et al., 2001; Meijer et al., 2001). Release of Ca, which serves as mediator during osmotic and ionic stress responses, is influenced by phosphoinositols and IP3 (Knight et al., 1997; Zhu, 2002). K1
Na1 interaction as well as K1 nutrient status regulates the normal functioning of cell. Interactions of K1
Na1 happens via selective uptake along with transportation of K1, into the shoot of the plants, independent of Na1 (Cramer et al., 1987). Enhanced ratio of K1/Na1 serves as a salt-tolerant trait in the leaves of several plant species as it influences nitrogen assimilation and photosynthetic activity (Chartzoulakis et al., 2002; Meena et al., 2003; Tabatabaei, 2006). In the shoots of plants especially in several woody species for avoiding the toxicity of Na1, its accumulation has been observed in the roots as an adaptive mechanism (Walker et al., 1987; Picchioni et al., 1990; Gucci and Tattini, 1997). Salt stress may also induce a decrease or an increase of Ca21, which depends on the nature and time duration of exposed stress and specific plant physiology as well (Gratten and Grieve, 1999; Unno et al., 2002; Ramoliya

Plant Life under Changing Environment

References

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et al., 2004; De Pascale et al., 2007). Integrity of plasma membrane is maintained by Ca as it limits the toxic effect of Na1 and plays an important role during stressed conditions as it acts as a secondary messenger during the cell’s signaling pathways (Rengel, 1992; Gucci and Tattini, 1997; Maathuis and Amtmann, 1999). Ca also regulates the Na1 influx and influence K1/Na1 selectivity via a nonselective ion channel. It also alleviates toxicity of salt in plants (Cramer et al., 1987; Rengel, 1992; Gucci and Tattini, 1997; Melgar et al., 2006; Sotiropoulos, 2007). Hence, it can be concluded that in plants an important criterion of stress tolerance could be higher tissue content of Ca21 and their ability of controlling the root-to-shoot transportation of Ca. In tolerance toward salinity stress, ratios of different cations such as Ca21/Na1 and K1/Na1 as an adaptive strategy were studied in woody/ nonwoody plants (Heimler et al., 1995; Maathuis and Amtmann, 1999; Dasgan et al., 2002). Many conifer species employ a freeze-drying mechanism to resist very low temperatures (260 C). Such protective strategies help in progressively removal of water during cooling from the plant’s tissues (Sakai, 1979). Both osmotic and salt stresses result in oxidative stress and cause severe impairment of plant seedling survival. In conclusion, ionomics approach has crucial roles in abiotic stress tolerance in plants.

References Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K., Yamaguchi Shinozaki, K., 2003. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activator in abscisic acid signalling. Plant Cell 15 (1), 63
78. Available from: https://doi.org/10.1105/tpc.006130. Abe, A., Kosugi, S., Yoshida, K., Natsume, S., Takagi, H., Kanzaki, H., et al., 2012. Genome sequencing reveals agronomically important loci in rice using MutMap. Nat. Biotechnol. 30, 174
178. Agarie, S., Shimoda, T., Shimizu, Y., Baumann, K., Sunagawa, H., Kondo, A., et al., 2007. Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum. J. Exp. Bot. 58, 1957
1967. Available from: https://doi.org/10.1093/jxb/erm057. Agarwal, S., Shaheen, R., 2007. Stimulation of antioxidant system and lipid peroxidation by abiotic stresses in leaves of Momordica charantia. Braz. J. Plant Physiol. 19 (2), 149
161. Available from: https://doi.org/10.1590/ S1677-04202007000200007. Ahmad, R., Lim, C.J., Kwon, S.Y., 2013. Glycine betaine: a versatile compound with great potential for gene pyramiding to improve crop plant performance against environmental stresses. Plant Biotechnol. Rep. 7, 49
57. Available from: https://doi.org/10.1007/s11816-012-0266-8. Askari, H., Edqvist, J., Hajheidari, M., Kafi, M., Salekdeh, G.H., 2006. Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics 6, 2542
2554. Available from: https://doi.org/10.1002/pmic.200500328. Baker, J., Steele, C., Dure III, L., 1988. Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol. Biol. U. S. A. 11, 277
291. Available from: https://doi.org/10.1007/BF00027385. Barberon, M., Vermeer, J.E., De Bellis, D., Wang, P., Naseer, S., Andersen, T.G., et al., 2016. Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164, 447
459. Baxter, I., Muthukumar, B., Park, H.C., Buchner, P., Lahner, B., Danku, J., et al., 2008. Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet. 4, e1000004. Baxter, I., Hosmani, P.S., Rus, A., Lahner, B., Borevitz, J.O., Muthukumar, B., et al., 2009. Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet. 5, e1000492. Baxter, I.R., Ziegler, G., Lahner, B., Mickelbart, M.V., Foley, R., Danku, J., et al., 2014. Single-kernel ionomic profiles are highly heritable indicators of genetic and environmental influences on elemental accumulation in maize grain (Zea mays). PLoS One 9, e87628. Binzel, M.L., 1995. NaCl-induced accumulation of tonoplast and plasma membrane H1-ATPase message in tomato. Physiol. Plant. 94, 722
728. Available from: https://doi.org/10.1111/j.1399-3054.1995.tb00990.x.

Plant Life under Changing Environment

850

35. Role of ionomics in plant abiotic stress tolerance

Blaylock, M.J., Huang, J.W., 2000. Phytoextraction of metals. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals-Using Plants to Clean Up the Environment. Wiley, New York, pp. 53
70. Boardman, R., McGuire, D.O., 1990. The role of zinc in forestry. I. Zinc in forest environments, ecosystems and tree nutrition. For. Ecol. Manage. 37, 167
205. Available from: https://doi.org/10.1016/0378-1127(90)90054-F. Bobrowicz, P., Wysocki, R., Owsianik, G., Goffeau, A., Ulaszewski, S., 1997. Isolation of three contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast 13, 819
828. Bonales-Alatorre, E., Shabala, S., Chen, Z., Pottosin, I.I., 2013. Reduced tonoplast FV and SV channels activity is essential for conferring salinity tolerance in a facultative halophyte, Chenopodium quinoa. Plant Physiol. 162, 940
952. Available from: https://doi.org/10.1104/pp.113.216572. Borghi, M., Rus, A., Salt, D.E., 2011. Loss-of-function of Constitutive Expresser of Pathogenesis Related Genes5 affects potassium homeostasis in Arabidopsis thaliana. PLoS One 6, e26360. Borkird, C., Simoems, C., Villarroel, R., Van Montagu, M., 1991. Gene expression associated with water-stress adaptation of rice cells and identification of two genes as hsp70 and ubiquitin. Physiol. Plant. 82, 449
457. Available from: https://doi.org/10.1111/j.1399-3054.1991.tb02931.x. Borsani, O., Valpuesta, V., Botella, M.A., 2001. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol. 126, 1024
1030. Available from: https://doi.org/10.1104/pp.126.3.1024. Bose, J., Rodrigo-Moreno, A., Lai, D., Xie, Y., Shen, W., Shabala, S., 2014. Rapid regulation of the plasma membrane H1-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann. Bot. 115, 481
494. Available from: https://doi.org/10.1093/aob/mcu219. Busk, P.K., Page`s, M., 1998. Regulation of abscisic acid-induced transcription. Plant Mol. Biol. 37, 425
435. Available from: https://doi.org/10.1023/A:1006058700720. Cailliatte, R., Lapeyre, B., Briat, J.F., Mari, S., Curie, C., 2009. The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem. J. 422, 217
228. Available from: https://doi.org/10.1042/BJ20090655. Cakmak, I., Marschner, H., 1992a. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol. 98, 1222
1227. Available from: https://doi.org/10.1104/pp.98.4.1222. Cakmak, I., Marschner, H., 1992b. Magnesium deficiency enhances resistance to paraquat toxicity in bean leaves. Plant Cell Environ. 15, 955
960. Available from: https://doi.org/10.1111/j.13653040.1992.tb01028.x. Cakmak, I., Marshner, H., 1993. Effect of zinc nutritional status on superoxide radical and hydrogen peroxide scavenging enzymes in bean leaves. In: Barrow, N.J. (Ed.), Plant Nutrition-From Genetic Engineering Field Practice. Kluwer, Dordrecht, pp. 133
137.. Available from: https://doi.org/10.1007/978-94-011-1880-4_21. Chao, D.Y., Gable, K., Chen, M., Baxter, I., Dietrich, C.R., Cahoon, E.B., et al., 2011. Sphingolipids in the root play an important role in regulating the leaf ionome in Arabidopsis thaliana. Plant Cell 23, 1061
1081. Chao, D.-Y., Silva, A., Baxter, I., Huang, Y.S., Nordborg, M., Danku, J., et al., 2012. Genome-wide association studies identify heavy metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLoS Biol. 8, e1002923. Available from: https://doi.org/10.1371/journal.pgen.1002923. Chao, D.Y., Dilkes, B., Luo, H., Douglas, A., Yakubova, E., Lahner, B., et al., 2013. Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341, 658
659. Chao, D.Y., Baraniecka, P., Danku, J., Koprivova, A., Lahner, B., Luo, H., et al., 2014a. Variation in sulfur and selenium accumulation is controlled by naturally occurring isoforms of the key sulfur assimilation enzyme Adenosine 50-Phosphosulfate Reductase2 across the Arabidopsis species range. Plant Physiol. 166, 1593
1608. Chao, D.Y., Chen, Y., Chen, J., Shi, S., Chen, Z., Wang, C., et al., 2014b. Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol. 12, e1002009. Available from: https://doi.org/10.1371/journal.pbio.1002009. Chartzoulakis, K., Loupassaki, M., Bertaki, M., Androulakis, I., 2002. Effects of NaCl salinity on growth, ion content and CO2 assimilation rate of six olive cultivars. Sci. Hortic. 96, 235
247. Available from: https://doi.org/ 10.1016/j.agwat.2005.04.025. Chen, Z., Shinano, T., Ezawa, T., Wasaki, J., Kimura, K., Osaki, M., et al., 2009a. Elemental interconnections in Lotus japonicus, a systematic study of the effects of elements additions on different natural variants. Soil Sci. Plant Nutr. 55, 91
101. Chen, Z., Watanabe, T., Shinano, T., Osaki, M., 2009b. Rapid characterization of plant mutants with an altered ion-profile: a case study using Lotus japonicus. New Phytol. 181, 795
801.

Plant Life under Changing Environment

References

851

Cramer, G.R., Lynch, J., La¨uchli, A., Epstein, E., 1987. Influx of Na1, K1, and Ca21 into roots of salt stressed cotton seedlings. Effects of supplemental Ca21. Plant Physiol. 83, 510
516. Available from: https://doi.org/10.1104/ pp.83.3.510. Das, P., Samantaray, S., Rout, G.R., 1997. Studies on cadmium toxicity in plants: a review. Environ. Pollut. 98, 29
36. Available from: https://doi.org/10.1016/S0269-7491(97)00110-3. Dasgan, H.Y., Aktas, H., Abak, K., Cakmak, I., 2002. Determination of screening techniques to salinity tolerance in tomatoes and investigation of genotype responses. Plant Sci. 163, 695
703. Available from: https://doi.org/ 10.1016/S0168-9452(02)00091-2. De Pascale, S., Martino, A., Raimondi, G., Maggio, A., 2007. Comparative analysis of water and salt stress-induced modifications of quality parameters in cherry tomatoes. J. Hortic. Sci. Biotechnol. 82 (2), 283
289. Available from: https://doi.org/10.1080/14620316.2007.11512230. DeWald, D.B., Torabinejad, J., Jones, C.A., Shope, J.C., Cangelosi, A.R., Thompson, J.E., Prestwich, G.D., Hama, H., 2001. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol. 126, 759
769. Available from: https://doi.org/10.1104/pp.126.2.759. Du, C.X., Fan, H.F., Guo, S.R., Tezuka, T., Li, J., 2010. Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochemistry 71, 1450
1459. Available from: https://doi.org/10.1016/j.phytochem.2010.05.020. Duan, G.-L., Zhou, Y., Tong, Y.-P., Mukhopadhyay, R., Rosen, B.P., Zhu, Y.G., 2007. A CDC25 homologue from rice functions as an arsenate reductase. New Phytol. 174, 311
321. Available from: https://doi.org/10.1111/ j.1469-8137.2007.02009.x. Dure III, L., Crouch, M., Harada, J., Ho, T.-H.D., Mundy, J., Quatrano, R., et al., 1989. Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol. Biol. 12, 475
486. Available from: https://doi.org/10.1007/BF00036962. Ebbs, S.D., Kochian, L.V., 1997. Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J. Environ. Qual. 26, 776
781. Available from: https://doi.org/10.2134/jeq1997.00472425002600030026x. Eide, D., Broderius, M., Fett, J., Guerinot, M.L., 1996. A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. U. S. A. 93, 5624
5628. Available from: https:// doi.org/10.1073/pnas.93.11.5624. Elansary, H.O., Yessoufou, K., Abdel-Hamid, A.M.E., El-Esawi, M.A., Ali, H.M., Elshikh, M.S., 2017. Seaweed Extracts Enhance Salam Turfgrass Performance during Prolonged Irrigation Intervals and Saline Shock. Front. Plant Sci. 8, 830. Elansary, H.O., Szopa, A., Kubica, P., Ekiert, H., Ali, H.M., Elshikh, M.S., et al., 2018. Bioactivities of traditional medicinal plants in Alexandria. Evid. Based Complement. Alternat. Med. 1
13. El-Esawi, M.A., 2016a. Micropropagation technology and its applications for crop improvement. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 523
545. El-Esawi, M.A., 2016b. Nonzygotic embryogenesis for plant development. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 583
598. El-Esawi, M.A., 2016c. Somatic hybridization and microspore culture in Brassica improvement. In: Anis, M., Ahmad, N. (Eds.), Plant Tissue Culture: Propagation, Conservation and Crop Improvement. Springer, Singapore, pp. 599
609. El-Esawi, M.A., 2017a. Genetic diversity and evolution of Brassica genetic resources: From morphology to novel genomic technologies-A review. Plant Genet. Resour. 15, 388
399. El-Esawi, M.A., 2017b. SSR analysis of genetic diversity and structure of the germplasm of faba bean (Vicia faba L.). Comptes Rendus Biol. 340, 474
480. El-Esawi, M.A., Alayafi, A.A., 2017a. Overexpression of Rice Rab7 Gene Improves Drought and Heat Tolerance and Increases Grain Yield in Rice (Oryza sativa L.). Genes 10, 56. El-Esawi, M.A., Alayafi, A.A., 2019b. Overexpression of StDREB2 Transcription Factor Enhances Drought Stress Tolerance in Cotton (Gossypium barbadense L.). Genes 10, 142. El-Esawi, M.A., Sammour, R., 2014. Karyological and phylogenetic studies in the genus Lactuca L. (asteraceae). Cytologia 79, 269
275. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Alayafi, A.A., Witczak, J., Ahmad, M., 2018a. Analysis of Genetic Variation and Enhancement of Salt Tolerance in French Pea (Pisum Sativum L.). Int. J. Mol. Sci. 19, 2433.

Plant Life under Changing Environment

852

35. Role of ionomics in plant abiotic stress tolerance

El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Ali, H.M., Alayafi, A.A., Witczak, J., et al., 2018b. Genetic Variation and Alleviation of Salinity Stress in Barley (Hordeum vulgare L.). Molecules 23, 2488. El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Alamri, S.A., Ali, H.M., Alayafi, A.A., 2018c. Bacillus firmus (SW5) augments salt tolerance in soybean (Glycine max L.) by modulating root system architecture, antioxidant defense systems and stress-responsive genes expression. Plant Physiol. Biochem. 132, 375
384. El-Esawi, M.A., Alaraidh, I.A., Alsahli, A.A., Alzahrani, S.M., Ali, H.M., Alayafi, A.A., et al., 2018d. Serratia liquefaciens KM4 Improves Salt Stress Tolerance in Maize by Regulating Redox Potential, Ion Homeostasis, Leaf Gas Exchange and Stress-Related Gene Expression. Int. J. Mol. Sci. 19, 3310. El-Esawi, M.A., Elansary, H.O., El-Shanhorey, N.A., Abdel-Hamid, A.M.E., Ali, H.M., Elshikh, M.S., 2017a. Salicylic Acid-Regulated Antioxidant Mechanisms and Gene Expression Enhance Rosemary Performance under Saline Conditions. Front. Physiol. 8, 716. El-Esawi, M., Arthaut, L., Jourdan, N., d’Harlingue, A., Martino, C., Ahmad, M., 2017b. Blue-light induced biosynthesis of ROS contributes to the signaling mechanism of Arabidopsis cryptochrome. Sci. Rep. 7, 13875. El-Esawi, M.A., Elkelish, A., Elansary, H.O., Ali, H.M., Elshikh, M., Witczak, I., et al., 2017c. Genetic Transformation and Hairy Root Induction Enhance the Antioxidant Potential of Lactuca serriola L. Oxidative Medicine and Cellular Longevity 2017, Article ID 5604746, 8 pages. El-Esawi, M.A., Germaine, K., Bourke, P., Malone, R., 2016a. Genetic diversity and population structure of Brassica oleracea germplasm in Ireland using SSR markers. Comptes Rendus Biol. 339, 133
140. El-Esawi, M.A., Germaine, K., Bourke, P., Malone, R., 2016b. AFLP analysis of genetic diversity and phylogenetic relationships of Brassica oleracea in Ireland. Comptes Rendus Biol. 339, 163
170. El-Esawi, M., Glascoe, A., Engle, D., Ritz, T., Link, J., Ahmad, M., 2015. Cellular metabolites modulate in vivo signaling of Arabidopsis cryptochrome-1. Plant Signal. Behav. 10, e1063758. El-Esawi, M.A., Mustafa, A., Badr, S., Sammour, R., 2017d. Isozyme analysis of genetic variability and population structure of Lactuca L. germplasm. Biochem. Syst. Ecol. 70, 73
79. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Alayafi, A.A., 2019a. Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stressrelated genes expression. Environ. Exp. Bot. 159, 55
65. El-Esawi, M.A., Al-Ghamdi, A.A., Ali, H.M., Ahmad, M., 2019b. Overexpression of AtWRKY30 Transcription Factor Enhances Heat and Drought Stress Tolerance in Wheat (Triticum aestivum L.). Genes 10, 163. Elkelish, A.A., Soliman, M.H., Alhaithloul, H.A., El-Esawi, M.A., 2019. Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiol. Bioch. 137, 144
153. Ellis, D.R., Gumaelius, L., Indriolo, E., Pickering, I.J., Banks, J.A., Salt, D.E., 2006. A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol. 141, 1544
1554. Available from: https://doi. org/10.1104/pp.106.084079. El-Shintinawy, F., El-Shourbagy, M.N., 2001. Alleviation of changes in protein metabolism in NaCl-stressed wheat seedlings by thiamine. Biol. Plant. 44, 541
545. Available from: https://doi.org/10.1023/A:1013738603020. Fernandez-Garcia, N., Hernandez, M., Casado-vela, J., Bru, R., Elortza, F., Hedden, P., et al., 2011. Changes to the proteome and targeted metabolites of xylem sap in Brassica oleracea in response to salt stress. Plant Cell Environ. 34, 821
836. Available from: https://doi.org/10.1111/j.1365-3040.2011.02285.x. Finkelstein, R.R., Gampala, S.S., Rock, C.D., 2002. Abscisic acid signaling in seeds and seedlings. Plant Cell 14, S15
S45. Available from: https://doi.org/10.1105/tpc.010441. Flowers, T.J., 2004. Improving crop salt tolerance. J. Exp. Bot. 55, 307
319. Available from: https://doi.org/ 10.1093/jxb/erh00. Flowers, T.J., Colmer, T.D., 2008. Salinity tolerance in halophytes. Tansley Rev. New Phytol. 179, 945
963. Available from: https://doi.org/10.1111/j.1469-8137.2008.02531.x. Fontes, R.L.S., Cox, F.R., 1998. Zinc toxicity in soybean grown at high iron concentration in nutrient solution. J. Plant. Nutr. 21, 1723
1730. Available from: https://doi.org/10.1080/01904169809365517. Forsberg, S.K.G., Andreatta, M.E., Huang, X.-Y., Danku, J., Salt, D.E., Carlborg, O., 2015. The multi-allelic genetic architecture of a variance-heterogeneity locus for molybdenum concentration in leaves acts as a source of unexplained additive genetic variance. PLoS Genet. 11, e1005648. Foy, C.D., 1978. The physiology of metal toxicity in plants. Ann. Rev. Plant Physiol. 29, 511
566. Available from: https://doi.org/10.1146/annurev.pp.29.060178.002455.

Plant Life under Changing Environment

References

853

Foy, C.D., Weil, R.R., Coradetti, C.A., 1995. Differential manganese tolerances of cotton genotypes in nutrient solution. J. Plant Nutr. 18, 685
706. Available from: https://doi.org/10.1080/01904169509364931. Franke, R.B., 2015. Caspary’s conductor. Proc. Natl. Acad. Sci. U. S. A. 112, 10084
10085. Fujita, Y., Fujita, M., Shinozaki, K., Yamaguchi-Shinozaki, K., 2011. ABA-mediated transcriptional regulation in response to osmotic stress in plants. J. Plant Res. 124, 509
525. Available from: https://doi.org/10.1007/s10265-011-0412-3. Go´mez-Porras, J.L., Rian˜o-Pacho´n, D.M., Dreyer, I., Mayer, J.E., Mueller-Roeber, B., 2007. Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC Genomics 8, 260. Available from: https://doi.org/10.1186/1471-2164-8-260. Gagneul, D., Alnouche, A., Duhaze´, C., Lugan, R., Larher, F.R., Bouchereau, A., 2007. A reassessment of the function of the so-called compatible solutes in the halophytic plumbaginaceae Limonium latifolium. Plant Physiol. 144, 1598
1611. Available from: https://doi.org/10.1104/pp.107.099820. Geldner, N., 2013. The endodermis. Annu. Rev. Plant Biol. 64, 531
558. Ghosh, M., Shen, J., Rosen, B.P., 1999. Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 96, 5001
5006. Available from: https://doi.org/10.1073/pnas.96.9.5001. Golldack, D., Dietz, K.-J., 2001. Salt-induced expression of the vacuolar H1-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol. 125 (4), 1643
1654. Available from: https://doi. org/10.1104/pp.125.4.164. Gong, Q., Li, P., Ma, S., Rupassara, S.I., Bohnert, H., 2005. Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant Physiol. 44, 826
839. Available from: https://doi.org/10.1111/j.1365-313X.2005.02587.x. Gratten, S.R., Grieve, C.M., 1999. Salinity mineral nutrient relation in horticultural crops. Sci. Hortic. 78, 127
157. Available from: https://doi.org/10.1016/S0304-4238(98)00192-7. Grennan, A.K., 2009. Identification of genes involved in metal transport in plants. Plant Physiol. 149, 1623
1624. Available from: https://doi.org/10.1104/pp.109.900287. Gucci, R., Tattini, M., 1997. Salinity tolerance in olive. In: Janik, J. (Ed.), Horticultural reviews. Wiley, New York, pp. 177
214. Guo, J., Dai, X., Wu, W., Ma, M., 2008. Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere. 72, 1020
1026. Available from: https://doi.org/10.1016/j.chemosphere.2008.04.018. Gu, R., Chen, F., Liu, B., Wang, X., Liu, J., Li, P., et al., 2015. Comprehensive phenotypic analysis and quantitative trait locus identification for grain mineral concentration, content, and yield in maize (Zea mays L.). Theor. Appl. Genet. 128, 1777
1789. Gustin, J.L., Zanis, M.J., Salt, D.E., 2011. Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol. Biol. 11, 76. Available from: https://doi.org/10.1186/1471-2148-11-76. Hall, J.L., Williams, L.E., 2003. Transition metal transporters in plants. J. Exp. Bot. 54, 2601
2613. Available from: https://doi.org/10.1093/jxb/erg303. Halliwell, B., Cutteridge, J.M.C., 1990. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 186, 1
85. Available from: https://doi.org/10.1016/0076-6879(90)86093-B. Halpin, C., 2013. Cell biology: up against the wall. Curr. Biol. 23, R1048
R1050. Haney, C.J., Grass, G., Franke, S., Rensing, C., 2005. New developments in the understanding of the cation diffusion facilitator family. J. Ind. Microbiol. Biotechnol. 32, 215
226. Available from: https://doi.org/10.1007/s10295-005-0224-3. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J., 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Mol. Biol. 51, 463
499. Available from: https://doi.org/10.1016/S1360-1385(00) 01692-7. Hattori, T., Totsuka, M., Hobo, T., Kagaya, Y., Yamamoto-Toyoda, A., 2002. Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant Cell Physiol. 43, 136
140. Available from: https://doi.org/10.1093/pcp/pcf014. Heimler, D., Tatini, M., Tici, S., Coradeshi, M.A., Traversi, M.L., 1995. Growth, ion accumulation and lipid composition of two olive genotypes under salinity. J. Plant Nutr. 18, 1723
1734. Available from: https://doi.org/ 10.1080/01904169509365017. Hernandez, L.E., sCarpena-Ruiz, R., Garate, A., 1996. Alterations in the mineral nutrition of pea seedlings exposed to cadmium. J. Plant Nutr. 19, 1581
1598. Available from: https://doi.org/10.1080/01904169609365223. Hinkle, P.M., Kinsella, P.A., Osterhoudt, K.C., 1987. Cadmium uptake and toxicity via voltage-sensitive calcium channels. J. Biol. Chem. 262, 16333
16337.

Plant Life under Changing Environment

854

35. Role of ionomics in plant abiotic stress tolerance

Hosmani, P.S., Kamiya, T., Danku, J., Naseer, S., Geldner, N., Guerinot, M.L., et al., 2013. Dirigent domaincontaining protein is part of the machinery required for formation of the lignin based Casparian strip in the root. Proc. Natl. Acad. Sci. U. S. A. 110, 14498
14503. Huang, X.-Y., Salt, D.E., 2016. Plant ionomics: from elemental profiling to environmental adaptation. Mol. Plant 9, 787
797. Hurkman, W.J., Tanaka, C.K., 1988. Poly-peptide changes induced by salt stress, water deficit, and osmotic stress in barley roots: a comparison using two-dimensional gel electro-phoresis. Electrophoresis 9, 781
787. Available from: https://doi.org/10.1002/elps.1150091114. Hurkman, W.J., Tanaka, C.K., DuPont, F.M., 1988. The effects of salt stress on polypeptides in membrane fractions from barley roots. Plant Physiol. 88, 1263
1273. Available from: https://doi.org/10.1104/pp.88.4.1263. Hussain, D., Haydon, M.J., Wang, Y., Wong, E., Sherson, S.M., Young, J., et al., 2004. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16, 1327
1339. Available from: https://doi.org/10.1105/tpc.020487. Illan, Y.A., Crapski, C., Meisel, D., 1976. The one-electron transfer redox potentials of free radicals. The oxygen/superoxide system. Biochim. Biophys. Acta 430, 209
224. Available from: https://doi.org/10.1016/0005-2728(76)90080-3. Kamiya, T., Borghi, M., Wang, P., Danku, J.M., Kalmbach, L., Hosmani, P.S., et al., 2015. The MYB36 transcription factor orchestrates Casparian strip formation. Proc. Natl. Acad. Sci. U. S. A. 112, 10533
10538. Karez, C.S., Allemand, D., De Renzis, G., Gnassia-Barelli, M., Romeo, M., Puiseux-Dao, S., 1990. Ca-Cd interaction in the prymnesiophyte Cricosphaera elongata. Plant Cell Environ. 13, 483
487. Available from: https://doi.org/ 10.1111/j.1365-3040.1990.tb01326.x. Kawano, T., Kawano, N., Muto, S., Lapeyrie, F., 2001. Cation-induced superoxide generation in tobacco cell suspension culture is dependent on ion valence. Plant Cell Environ. 24, 1235
1241. Available from: https://doi. org/10.1046/j.1365-3040.2001.00766.x. Khan, M.S., 2011. Role of sodium and hydrogen (Na1/H1) antiporters in salt tolerance of plants: present and future challenges. Afr. J. Biotechnol. 10, 13693
13704. Available from: https://doi.org/10.5897/AJB11.1630. Knight, H., Trewavas, A.J., Knight, M.R., 1997. Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 12 (5), 1067
1078. Available from: https://doi.org/10.1046/j.1365-313x.1997.12051067.x. Kononowicz, A.K., Nelson, D.E., Singh, N.K., Hasegawa, P.M., Bressan, R.A., 1992. Regulation of the osmotin gene promoter. Plant Cell 4, 513
524. Available from: https://doi.org/10.1105/tpc.4.5.513. Koprivova, A., Giovannetti, M., Baraniecka, P., Lee, B.R., Grondin, C., Loudet, O., et al., 2013. Natural variation in the ATPS1 isoform of ATP sulfurylase contributes to the control of sulfate levels in Arabidopsis. Plant Physiol. 163, 1133
1141. Koyro, H.W., 1997. Ultrastructural and physiological changes in root cells of Sorghum plants (Sorghum bicolor 3 S. sudanensis cv Sweet Sioux) induced by NaCl. J. Exp. Bot. 48, 693
706. Available from: https://doi.org/ 10.1093/jxb/48.3.693. Lahner, B., Gong, J.M., Mahmoudian, M., Smith, E.L., Abid, K.B., Rogers, E.E., et al., 2003. Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat. Biotechnol. 21, 1215
1221. Landrieu, I., da Costa, M., De Veylder, L., Dewitte, F., Vandepoele, K., Hassan, S., et al., 2004a. A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 101, 13380
13385. Available from: https://doi.org/10.1073/pnas.0405248101. Landrieu, I., Hassan, S., Sauty, M., Dewitte, F., Wieruszeski, J.M., Inze´, D., et al., 2004b. Characterization of the Arabidopsis thaliana Arath; CDC25 dual specificity tyrosine phosphatase. Biochem. Biophys. Res. Commun. 322, 734
739. Available from: https://doi.org/10.1016/j.bbrc.2004.07.182. LaRosa, P.C., Singh, N.K., Hasegawa, P.M., Bressan, R.A., 1989. Stable NaCl tolerance of tobacco cells is associated with enhanced accumulation of osmotin. Plant Physiol. 91, 855
861. Available from: https://doi.org/10.1104/ pp.91.3.855. Lenntech Water Treatment and Air Purification, 2004. Water treatment. Lenntech, Rotterdamseweg. ,http:// www.excelwater.com/thp/filters/WaterPurification.Htm.. Lewis, S., Donkin, M.E., Depledge, M.H., 2001. Hsp 70 expression in Enteromorpha intestinalis (Chlorophyta) exposed to environmental stressors. Aquat. Toxicol. 51, 277
291. Available from: https://doi.org/10.1016/ S0166-445X(00)00119-3. Li, B., He, L., Guo, S., Guo, S., Li, J., Yang, Y., et al., 2013. Proteomics reveal cucumber Spd-responses under normal condition and salt stress. Plant Physiol. Biochem. 67, 7
14. Available from: https://doi.org/10.1016/j. plaphy.2013.02.016.

Plant Life under Changing Environment

References

855

Lin, Y.F., Liang, H.M., Yang, S.Y., Boch, A., Clemens, S., Chen, C.C., et al., 2009. Arabidopsis IRT3 is a zincregulated and plasma membrane localized zinc/iron transporter. New Phytol. 182, 392
404. Available from: https://doi.org/10.1111/j.1469-8137.2009.02766.x. Loudet, O., Saliba-Colombani, V., Camilleri, C., Calenge, F., Gaudon, V., Koprivova, A., et al., 2007. Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat. Genet. 39, 896
900. Ma, J.F., Yamaji, N., Mitani, N., Xu, X.Y., Su, Y.H., McGrath, S.P., et al., 2008. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc. Natl. Acad. Sci. U. S. A. 105, 9931
9935. Available from: https://doi.org/10.1073/pnas.0802361105. Maathuis, F.J.M., Amtmann, A., 1999. K1 nutrition and Na1 toxicity: the basis of cellular K1/Na1 ratios. Ann. Bot. 84, 123
133. Available from: https://doi.org/10.1006/anbo.1999.0912. Maathuis, F.J.M., 2006. The role of monovalent cation transporters in plant responses to salinity. J. Exp. Bot. 57, 1137
1147. Available from: https://doi.org/10.1093/jxb/erj001. Mahajan, S., Tuteja, N., 2005. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139
158. Available from: https://doi.org/10.1016/j.abb.2005.10.018. Maruyama, K., Todaka, D., Mizoi, J., Yohisda, T., Kidokoro, S., Matsukura, S., et al., 2012. Identification of cisacting promoter elements in cold-dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res. 19, 37
49. Available from: https://doi.org/10.1093/dnares/dsr040. Meena, S.K., Gupta, N.K., Gupta, S., Khandelwal, S.K., Sastry, E.V.D., 2003. Effect of sodium chloride on the growth and gas exchange of young Ziziphus seedling rootstocks. J. Hortic. Sci. Biotechnol. 78 (4), 454
457. Available from: https://doi.org/10.1080/14620316.2003.11511649. Meijer, H.J.G., Berrie, C.P., Iurisci, C., Divecha, N., Musgrave, A., Munnik, T., 2001. Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtIns5P), and its accumulation upon osmotic stress. Biochem. J. 360, 491
498. Available from: https://doi.org/10.1042/0264-6021:3600491. Melgar, J.C., Benlloch, M., Fernandez-Escobar, R., 2006. Calcium increases sodium exclusion in olive plants. Sci. Hortic. 109, 303
305. Available from: https://doi.org/10.1016/j.scienta.2006.04.013. Mills, R.F., Francini, A., da Rocha, P.S.C.F., Baccarini, P.J., Aylett, M., Krijger, G.C., et al., 2005. The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett. 579, 783
791. Available from: https://doi.org/10.1016/j.febslet.2004.12.040. Milner, M.J., Seamon, J., Craft, E., Kochian, L.V., 2013. Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J. Exp. Bot. 64, 369
381. Available from: https://doi.org/ 10.1093/jxb/ers315. Mohanpuria, P., Rana, N.K., Yadav, S.K., 2007. Cadmium induced oxidative stress influence on glutathione metabolic genes of Camellia sinensis (L.) O. Kuntze. Environ. Toxicol. 22, 368
374. Available from: https://doi.org/ 10.1002/tox.20273. Monni, S., Salemma, M., Millar, N., 2000. The tolerance of Empetrum nigrum to copper and nickel. Environ. Pollut. 109, 221
229. Available from: https://doi.org/10.1016/S0269-7491(99)00264-X. Morrissey, J., Baxter, I.R., Lee, J., Li, L., Lahner, B., Grotz, N., et al., 2009. The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21, 3326
3338. Mundy, J., Yamaguchi-Shinozaki, K., Chua, N.H., 1990. Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc. Natl. Acad. Sci. U. S. A. 87, 1406
1410. Available from: https://doi.org/10.1073/pnas.87.4.1406. Munir, N., Aftab, F., 2011. Enhancement of salt tolerance in sugarcane by ascorbic acid pretreatment. Afr. J. Biotechnol. 10 (80), 18362
18370. Available from: https://doi.org/10.5897/AJB11.2919. Munns, R., 2002. Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239
250. Available from: https://doi.org/10.1046/j.0016-8025.2001.00808.x. Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651
681. Available from: https://doi.org/10.1146/annurev.arplant.59.032607.092911. Nies, D.H., Silver, S., 1995. Ion efflux systems involved in bacterial metal resistances. J. Ind. Microbiol. 14, 186
199. Available from: https://doi.org/10.1007/BF01569902. Niu, X., Narasimhan, M.L., Salzman, R.A., Bressan, R.A., Hasegawa, P.M., 1993a. NaCl regulation of plasma membrane H1-ATPase gene expression in a glycophyte and a halophyte. Plant Physiol. 103, 713
718. Available from: https://doi.org/10.1104/pp.103.3.713.

Plant Life under Changing Environment

856

35. Role of ionomics in plant abiotic stress tolerance

Niu, X., Zhu, J.-K., Narasimhan, M.L., Bressan, R.A., Hasegawa, P.M., 1993b. Plasma membrane H1-ATPase gene expression is regulated by NaCl in cells of the halophyte Atriplex nummularia L. Planta 190, 433
438. Available from: https://doi.org/10.1007/BF00224780. Parent, S.E., Parent, L.E., Egozcue, J.J., Rozane, D.E., Hernandes, A., Lapointe, L., et al., 2013. The plant ionome revisited by the nutrient balance concept. Front. Plant Sci. 4, 39. Parida, A.K., Das, A.B., 2005. Salt tolerance and salinity effect on plants: a review. Ecotoxicol. Environ. Saf. 60, 324
349. Available from: https://doi.org/10.1016/j.ecoenv.2004.06.010. Parida, A.K., Das, A.B., Das, P., 2002. NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. J. Plant Biol. 45, 28
36. Available from: https://doi.org/10.1007/BF03030429. Patra, M., Sharma, A., 2000. Mercury toxicity in plants. Bot. Rev. 66, 379
422. Available from: https://doi.org/ 10.1007/BF02868923. Pfister, A., Barberon, M., Alassimone, J., Kalmbach, L., Lee, Y., Vermeer, J.E., et al., 2014. A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. Elife 3, e03115. Pical, C., Westergren, T., Dove, S.K., Larsson, C., Sommarin, M., 1999. Salinity and hyperosmotic stress induce rapid increases in phosphatidylinositol 4,5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in Arabidopsis thaliana cells. J. Biol. Chem. 274, 38232
38240. Available from: https://doi.org/10.1074/ jbc.274.53.38232. Picchioni, G.A., Miyamoto, S., Storey, J.B., 1990. Salt effects on growth and ion uptake of pistachio rootstock seedlings. J. Am. Soc. Hortic. Sci. 115, 647
653. Available from: https://doi.org/10.21273/JASHS.115.4.647. Pinson, S.R.M., Tarpley, L., Yan, W., Yeater, K., Lahner, B., Yakubova, E., et al., 2015. Worldwide genetic diversity for mineral element concentrations in rice grain. Crop Sci. 55, 294
311. Podar, D., Scherer, J., Noordally, Z., Herzyk, P., Nies, D., Sanders, D., 2012. Metal selectivity determinants in a family of transition metal transporters. J. Biol. Chem. 287, 3185
3196. Available from: https://doi.org/ 10.1074/jbc.m111.305649. Pourrut, B., Shahid, M., Dumat, C., Winterton, P., Pinelli, E., 2011. Lead uptake, toxicity, and detoxification in plants. In: Whitacre, D.M. (Ed.), Reviews of Environmental Contamination and Toxicology. Springer, New York, pp. 113
136. Available from: https://doi.org/10.1007/978-1-4419-9860-6_4. Prasad, M.N.V., Hagmeyer, J., 1999. Heavy Metal Stress in 1515 Plants. Springer, Berlin, pp. 16
20. Available from: https://doi.org/10.1007/978-3-662-07745-0. Ramoliya, P.J., Patel, H.M., Pandey, A.N., 2004. Effect of salinization of soil on growth and macro- and micronutrient accumulation in seedlings of Salvadora persica (Salvadoraceae). Forest Ecol. Manag. 202, 181
193. Available from: https://doi.org/10.1016/j.foreco.2004.07.020. Rea, P.A., 2003. Ion genomics. Nat. Biotechnol. 21, 1149
1151. Reeves, R.D., Baker, A.J.M., 2000. Metal-accumulating plants. In: Raskin, I., Ensley, B.D. (Eds.), Phytoremediation of Toxic Metals: Using Plants to Clean Up the Environment. Wiley, New York, pp. 193
229. Rengel, Z., 1992. The role of calcium in salt toxicity. Plant Cell Environ. 15, 625
632. Available from: https://doi. org/10.1111/j.1365-3040.1992.tb01004.x. Rhodes, D., 1987. Metabolic responses to stress. In: Davies, D.D. (Ed.), Physiology of Metabolism: A Comprehensive Treatise. Academic Press, New York, pp. 201
241. Ricachenevsky, F.K., Menguer, P.K., Sperotto, R.A., Williams, L.E., Fett, J.P., 2013. Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Front. Plant Sci. 4, 144. Available from: https://doi.org/10.3389/fpls.2013.00144. Roy, M., Wu, R., 2002. Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci. 163 (5), 987
992. Available from: https://doi. org/10.1016/S0168-9452(02)00272-8. Rus, A., Baxter, I., Muthukumar, B., Gustin, J., Lahner, B., Yakubova, E., et al., 2006. Natural variants of AtHKT1 enhance Na1 accumulation in two wild populations of Arabidopsis. PLoS Genet. 2, e210. Sagardoy, R., Va´zquez, S., Florez-Sarasa, I.D., Albacete, A., Ribas-Carbo´, M., Flexas, J., Abadı´a, J., Morales, F., 2010. Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytol. 187, 145
158. Available from: https://doi.org/ 10.1111/j.1469-8137.2010.03241.x.

Plant Life under Changing Environment

References

857

Sakai, A., 1979. Freezing avoidance mechanism of primordial shoots of conifer buds. Plant Cell Physiol. 20, 1381
1390. Available from: https://doi.org/10.1093/oxfordjournals.pcp.a075937. Salt, D.E., Baxter, I., Lahner, B., 2008. Ionomics and the study of the plant ionome. Annu. Rev. Plant Biol. 59, 709
733. Available from: https://doi.org/10.1146/annurev.arplant.59.032607.092942. Sanadhya, P., Agarwal, P., Agarwal, P.K., 2015. Ion homeostasis in a salt secreting halophytic grass. AoB Plants 7, plv055. Available from: https://doi.org/10.1093/aobpla/plv055. Sanchez, D.H., Siahpoosh, M.R., Roessner, U., Udvardi, M., Kopka, J., 2008. Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiol. Plant. 132, 209
219. Available from: https://doi.org/ 10.1111/j.1399-3054.2007.00993.x. Sanchez, D.H., Pieckenstain, F.L., Escaray, F., Erban, A., Kraemer, U.T.E., Udvardi, M.K., et al., 2011. Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis. Plant Cell Environ. 34, 605
617. Available from: https://doi.org/10.1111/ j.1365-3040.2010.02266.x. Sa´nchez-Bermejo, E., Castrillo, G., del Llano, B., Navarro, C., Zarco-Ferna´ndez, S., Martinez- Herrera, D.J., et al., 2014. Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana. Nat. Commun. 5, 4617. Available from: https://doi.org/10.1038/ncomms5617. Sa´nchez-Rodriguez, E., Rubio-Wilhelmi, M.D., Cervilla, L.M., Blasco, B., Rios, J.J., Leyva, R., et al., 2010. Study of the ionome and uptake fluxes in cherry tomato plants under moderate water stress conditions. Plant Soil 335, 339
347. Sasaki, A., Yamaji, N., Yokosho, K., Ma, J.F., 2012. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24, 2155
2167. Available from: https://doi.org/10.1105/tpc.112.096925. Schreck, E., Foucault, Y., Sarret, G., Sobanska, S., Ce´cillon, L., Castrec-Rouelle, M., et al., 2012. Metal and metalloid foliar uptake by various plant species exposed to atmospheric industrial fallout: mechanisms involved for lead. Sci. Total Environ. 427-428, 253
262. Available from: https://doi.org/10.1016/j.scitotenv.2012.03.051. Seregin, I.V., Ivanov, V.B., 2001. Physiological aspects of cadmium and lead toxic effects on higher plants. Russ. J. Plant Physiol. 48, 523
544. Available from: https://doi.org/10.1023/A:1016719901147. Shabala, S.N., Mackay, A.S., 2011. Ion transport in halophytes. Adv. Bot. Res. 57, 151
187. Available from: https://doi.org/10.1016/B978-0-12-387692-8.00005-9. Shabala, S., Shabala, L., Barcelo, J., Poschenrieder, C., 2014. Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant Cell Environ. 37, 2216
2233. Available from: https://doi.org/10.1111/pce.12339. Shi, H., Quintero, F.J., Pardo, J.M., Zhu, J.K., 2002. The putative plasma membrane Na1/H1 antiporter SOS1 controls long-distance Na1 transport in plants. Plant Cell 14, 465
477. Available from: https://doi.org/10.1105/ tpc.010371. Shinozaki, K., Yamaguchi-Shinozaki, K., 2000. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3 (3), 217
223. Shulaev, V., Cortes, D., Miller, G., Mittler, R., 2008. Metabolomics for plant stress response. Physiol. Plant 132 (2), 199
208. Available from: https://doi.org/10.1111/j.1399-3054.2007.01025.x. Singh, S., Parihar, P., Singh, R., Singh, V.P., Prasad, S.M., 2016. Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front. Plant Sci. 6, 1143. Available from: https://doi.org/ 10.3389/fpls.2015.01143. Simo˜es, C.C., Melo, J.O., Magalhaes, J.V., Guimara˜es, C.T., 2012. Genetic and molecular mechanisms of aluminum tolerance in plants. Genet. Mol. Res. 11, 1949
1957. Available from: https://doi.org/10.4238/2012.July.19.14. Singh, R.P., Tripathi, R.D., Sinha, S.K., Maheshwari, R., Srivastava, H.S., 1997. Response of higher plants to lead contaminated environment. Chemosphere 34, 2467
2493. Available from: https://doi.org/10.1016/S0045-6535 (97)00087-8. Skriver, K., Mundy, J., 1990. Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2, 503
512. Available from: https://doi.org/10.1105/tpc.2.6.503. Slama, I., Abdelly, C., Bouchereau, A., Flowers, T., Savoure, A., 2015. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann. Bot. 115, 433
447. Available from: https://doi.org/10.1093/aob/mcu239. Slesak, I., Miszalski, Z., Karpinska, B., Niewiadomska, E., Ratajczak, R., Karpinski, S., 2002. Redox control of oxidative stress responses in the C-3-CAM intermediate plant Mesembryanthemum crystallinum. Plant Physiol. Biochem. 40, 669
677. Available from: https://doi.org/10.1016/S0981-9428(02)01409-2.

Plant Life under Changing Environment

858

35. Role of ionomics in plant abiotic stress tolerance

Smirnoff, N., Cumbes, Q.J., 1989. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 1057
1060. Available from: https://doi.org/10.1016/0031-9422(89)80182-7. Sobhanian, H., Aghaeib, K., Komatsu, S., 2011. Changes in the plant proteome resulting from salt stress: toward the creation of salt-tolerant crops. J. Proteomics 74, 1323
1337. Available from: https://doi.org/10.1016/j. jprot.2011.03.018. Song, W.-Y., Yamaki, T., Yamaji, N., Ko, D., Jung, K.H., Fujii-Kashino, M., et al., 2014. A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. PNAS 111, 15699
15704. Available from: https://doi. org/10.1073/pnas.1414968111. Sotiropoulos, T.E., 2007. Effect of NaCl and CaCl2 on growth and contents of minerals, chlorophyll, proline and sugars in apple rootstock M 4 cultured in vitro. Biol. Plant. 51 (1), 177
180. Available from: https://doi.org/ 10.1007/s10535-007-0035-7. Stadtman, E.R., 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalysed reactions. Annu. Rev. Biochem. 62, 797
821. Available from: https://doi.org/10.1146/annurev.bi.62.070193.004053. Stepien, P., Johnson, G.N., 2009. Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol. 149, 1154
1165. Available from: https://doi.org/10.1104/pp.108.132407. Su, H., Balderas, E., Vera-Estrella, R., Golldack, D., Quigley, F., Zhao, C., Pantoja, O., Bohnert, H.J., 2003. Expression of the cation transporter McHKT1 in a halophyte. Plant Mol. Biol. 52, 967
980. Available from: https://doi.org/10.1023/A:1025445612244. Surowy, T.K., Boyer, J.S., 1991. Low water potentials affect expression of genes encoding vegetative storage proteins and plasma membrane proton ATPase in soybean. Plant Mol. Biol. 16, 251
262. Available from: https:// doi.org/10.1007/BF00020556. Tabatabaei, S.J., 2006. Effects of salinity and N on growth, photosynthesis and N status of olive (Olea europaea L.) trees. Sci. Hortic. 108, 432
438. Available from: https://doi.org/10.1016/j.scienta.2006.02.016. Tada, Y., Kashimura, T., 2009. Proteomic analysis of salt-responsive proteins in the mangrove plant, Bruguiera gymnorhiza. Plant Cell Physiol. 50, 439
446. Available from: https://doi.org/10.1093/pcp/pcp002. Thomashow, M.F., 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571
599. Available from: https://doi.org/10.1146/annurev. arplant.50.1.571. Tian, H., Baxter, I.R., Lahner, B., Reinders, A., Salt, D.E., Ward, J.M., 2010. Arabidopsis NPCC6/NaKR1 is a phloem mobile metal binding protein necessary for phloem function and root meristem maintenance. Plant Cell 22, 3963
3979. Tomatsu, H., Takano, J., Takahashi, H., Watanabe-Takahashi, A., Shibagaki, N., Fujiwara, T., 2007. An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc. Natl. Acad. Sci. U. S. A. 104, 18807
18812. Unno, H., Maeda, Y., Yamamoto, S., Okamoto, M., Takenaga, H., 2002. Relationship between salt tolerance and Ca21 retention among plant species. Jpn. J. Soil. Sci. Plant. Nutr. 73, 715
718. Available from: https://doi.org/ 10.20710/dojo.73.6_715. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., Yamaguchi-Shinozaki, K., 2000. Novel Arabidopsis ZIP transcription factors involved in an abscisic-acid-dependent signal transduction pathway under drought and high salinity conditions. Proc. Natl. Acad. Sci. U. S. A. 97, 11632
11637. Available from: https://doi.org/ 10.1073/pnas.190309197. Upadhyaya, H., Sahoo, L., Panda, S.K., 2013. Molecular physiology of osmotic stress in plants. In: Rout, G.R., Das, A.B. (Eds.), Molecular Stress Physiology of Plants. Springer, India, pp. 179
192. Available from: https://doi. org/10.1007/978-81-322-0807-5_7.. Uzilday, B., Ozgur, R., Sekmen, A.H., Yildiztugay, E., Turkan, I., 2015. Changes in the alternative electron sinks and antioxidant defense in chloroplasts of the extreme halophyte Eutrema parvulum (Thellungiella parvula) under salinity. Ann. Bot. 115, 449
463. Available from: https://doi.org/10.1093/aob/mcu184. Uzu, G., Sobanska, S., Aliouane, Y., Pradere, P., Dumat, C., 2009. Study of lead phytoavailability for atmospheric industrial micronic and sub-micronic particles in relation with lead speciation. Environ. Pollut. 157, 1178
1185. Available from: https://doi.org/10.1016/j.envpol.2008.09.053.

Plant Life under Changing Environment

References

859

Uzu, G., Sobanska, S., Sarret, G., Mun˜oz, M., Dumat, C., 2010. Foliar lead uptake by lettuce exposed to atmospheric fallouts. Environ. Sci. Technol. 44, 1036
1042. Available from: https://doi.org/10.1021/es902190u. Vert, G., Barberon, M., Zelazny, E., Se´gue´la, M., Briat, J.F., Curie, C., 2009. Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta 229, 1171
1179. Available from: https://doi.org/10.1007/s00425-009-0904-8. Vierling, E., 1991. The role of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 579
620. Available from: https://doi.org/10.1146/annurev.pp.42.060191.003051. Vwioko, E., Adinkwu, O., El-Esawi, M.A., 2017. Comparative Physiological, Biochemical and Genetic Responses to Prolonged Waterlogging Stress in Okra and Maize Given Exogenous Ethylene Priming. Front. Physiol. 8, 632. Wakeel, A., Asif, A.R., Pitann, B., Schubert, S., 2011. Proteome analysis of sugar beet (Beta vulgaris L.) elucidates constitutive adaptation during the first phase of salt stress. J. Plant Physiol. 168, 519
526. Available from: https://doi.org/10.1016/j.jplph.2010.08.01. Walker, R.R., To¨ro¨kfalvy, E., Behboodian, M.H., 1987. Uptake and distribution of chloride, sodium and potassium ions and growth of salt-treated pistachio plants. Aust. J. Agric. Res. 38, 383
394. Available from: https://doi. org/10.1071/AR9870383. Wang, W.X., Barak, T., Vinocur, B., Shoseyov, O., Altman, A., 2007. Abiotic resistance and chaperones: possible physiological role of SP1, a stable and stabilizing protein from Populus. In: Vasil, I.K. (Ed.), Plant Biotechnology 2000 and Beyond, Kluwer, Dordrecht, pp. 439
443. Available from: https://doi.org/10.1007/978-94-017-2679-5_91. Warne, M.S., Heemsbergen, D., Stevens, D., McLaughlin, M., Cozens, G., Whatmuff, M., et al., 2008. Modeling the toxicity of copper and zinc salts to wheat in 14 soils. Environ. Toxicol. Chem. 27, 786
792. Available from: https://doi.org/10.1897/07-294.1. Watanabe, T., Broadley, M.R., Jansen, S., White, P.J., Takada, J., Satake, K., et al., 2007. Evolutionary control of leaf element composition in plants. New Phytol. 174, 516
523. Williams, L.E., Pittman, J.K., Hall, J.L., 2000. Emerging mechanisms for heavy metal transport in plants. Biochim. Biophys. Acta 1465, 104
126. Available from: https://doi.org/10.1016/S0005-2736(00)00133-4. Wintz, H., Fox, T., Vulpe, C., 2002. Responses of plants to iron, zinc and copper deficiencies. Biochem. Soc. Trans. 30, 766
768. Available from: https://doi.org/10.1042/bst0300766. Wong, C.K.E., Cobbett, C.S., 2009. HMA P-Type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol. 181, 71
78. Available from: https://doi.org/10.1111/j.14698137.2008.02638.x. Wu, D., Shen, Q., Cai, S., Chen, Z.H., Dai, F., Zhang, G., 2013. Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol. 54, 1976
1988. Xia, J., Yamaji, N., Kasai, T., Ma, J.F., 2010. Plasma membrane-localized transporter for aluminum in rice. Proc. Natl. Acad. Sci. USA. 107, 18381
18385. Available from: https://doi.org/10.1073/pnas.1004949107. Yamaguchi-Shinozaki, K., Shinozaki, K., 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781
803. Available from: https://doi.org/ 10.1146/annurev.arplant.57.032905.105444. Yu, J., Chen, S., Zhao, Q., Wang, T., Yang, C., Diaz, C., et al., 2011. Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J. Proteome Res. 10, 3852
3870. Available from: https://doi.org/10.1021/ pr101102p. Yuan, H.J., Ma, Q., Wu, G.Q., Wang, P., Hu, J., Wang, S.M., 2015. ZxNHX controls Na1 and K1 homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedback regulation of the expression of genes involved in their transport. Ann. Bot. 115, 495
507. Available from: https://doi.org/10.1093/aob/mcu177. Zhang, W., Ruan, J., Ho, T.H., You, Y., Yu, T., Quatrano, R.S., 2005. Cis-regulatory element based targeted gene finding: genome-wide identification of abscisic acid and abiotic stress-responsive genes in Arabidopsis thaliana. Bioinformatics 21, 3074
3081. Available from: https://doi.org/10.1093/bioinformatics/bti490. Zhang, Y., Fonslow, B.R., Shan, B., Baek, M.C., Yates III, J.R., 2013. Protein analysis by shotgun/bottom-up proteomics. Chem. Rev. 10, 234
294. Available from: https://doi.org/10.1021/cr3003533. Zhou, Z.S., Huang, S.Q., Guo, K., Mehta, S.K., Zhang, P.C., Yang, Z.M., 2007. Metabolic adaptations to mercuryinduced oxidative stress in roots of Medicago sativa L. J. Inorg. Biochem. 101, 1
9. Available from: https://doi. org/10.1016/j.jinorgbio.2006.05.011.

Plant Life under Changing Environment

860

35. Role of ionomics in plant abiotic stress tolerance

Zhu, J.K., 2002. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247
273. Available from: https://doi.org/10.1146/annurev.arplant.53.091401.143329. Zhu, J.-K., Shi, J., Bressan, R.A., Hasegawa, P.M., 1993. Expression of an Atriplex nummularia gene encoding a protein homologous to the bacterial molecular chaperone DnaJ. Plant Cell 5, 341
349. Available from: https:// doi.org/10.1105/tpc.5.3.341. Zhu, J.-K., Damsz, B., Kononowicz, A.A., Bressan, R.A., Hasegawa, P.M., 1994. A plant vitro nectin-like extracellular adhesion protein is related to the translational elongation factor-1 alpha. Plant Cell 6, 393
404. Available from: https://doi.org/10.1105/tpc.6.3.393. Ziegler, G., Terauchi, A., Becker, A., Armstrong, P., Hudson, K., Baxter, I., 2013. Ionomic screening of field-grown soybean identifies mutants with altered seed elemental composition. Plant Genome 6. Available from: https:// doi.org/10.3835/plantgenome2012.07.0012.

Further reading Indriolo, E., Na, G., Ellis, D., Salt, D.E., Banks, J.A., 2010. A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 22, 2045
2057. Available from: https://doi.org/10.1105/tpc.109.069773. Nanjo, T., Kobayashi, T.M., Yoshida, Y., Kakubari, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., 1999. Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett. 461, 205
210. Available from: https://doi.org/10.1016/S0014-5793(99)01451-9.

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C H A P T E R

36 Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture Ved Prakash1, Mohd Younus Khan1, Padmaja Rai1, Rajendra Prasad2, Durgesh Kumar Tripathi3 and Shivesh Sharma1 1

Department of Biotechnology, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India 2Department of Horticulture, Kulbhaskar Ashram Post Graduate College, Prayagraj, India 3Amity Institute of Organic Agriculture, Amity University Uttar Pradesh, Noida, India

36.1 Introduction Microbial diversity and number in the rhizospheric region is much higher when compared with bulk soil as the region gets nutrition via root exudation, competition for nutrients and provides support for growth, which makes the zone physiologically active. Microbial community associated with the plant is known as the second genome of the plant (Nichols et al., 1997; Baudoin et al., 2003; Berendsen et al., 2012). The plant growthpromoting rhizobacterias (PGPRs) can be employed as biofertilizers, bioinoculant, and biocontrol agents based upon the capability of their nitrogen fixation, ability to protect the plant against harmful microbes, respectively (Bloemberg and Lugtenberg, 2001). The residence period of PGPR lies for weeks in soils. Microbial consortia help the plant to withstand nutritional stress (Finkel et al., 2017). Factors, such as soil composition, pH, water level, temperature, and nature of root exudation, determine bacterial population in the rhizospheric region (Baudoin et al., 2003; Landa et al., 2004; Cakmakci et al., 2007). Microbial diversity within rhizosphere much depends upon its physical, chemical, and biological characteristics of soil, which determines the diversity and activity of microbiota within the rhizospheric zone

Plant Life under Changing Environment DOI: https://doi.org/10.1016/B978-0-12-818204-8.00040-0

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© 2020 Elsevier Inc. All rights reserved.

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36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

(Brimecombe et al., 2000; Kennedy, 1998). The commercial use of rhizobacteria can be implemented for the improvement of crop productivity under stressful environment as it has shown promising results in enhancing root development, supports biomass, and improves seedling growth (Nadeem et al., 2014; Hafeez et al., 2004; Weyens et al., 2009). PGPR confers various physiological attributes to plants by producing phytohormones such as indole-3acetic aldehyde (IAA), gibberellins, cytokinins, phosphate solubilization, siderophore production, hydrogen cyanide (HCN) production, and ACC deaminase production along with other valuable compounds (Van Peer et al., 1991; Garcı´a de Salamone et al., 2001; Joo et al., 2005; Flores-Vargas and O’hara, 2006; Orhan et al., 2006; Gupta and Gopal, 2008; Bal et al., 2013; Mohite, 2013; Gontia-Mishra et al., 2016). In metal-contaminated soil compared to traditional agricultural practice where agrochemicals are abruptly applied, PGPR maintains the soil fertility by detoxifying metal contamination and augments plant growth by producing compounds such as siderophores (Khan et al., 2009). Root-colonizing bacteria confer plants with tolerance capability against abiotic stresses such as salinity, drought, and heavy metal (de Zelicourt et al., 2013).

36.1.1 Growth attributes by plant growth-promoting rhizobacteria PGPR appeared as the microbes existing among the competitive microflora of a plant with inherent characteristics to colonize the root surface, divide and assist the plant growth (Kloepper, 1994). Approximately 2% 5% of microbial species exist in the rhizospheric region possessing plant growth-promoting (PGP) capabilities (Kloepper, 1978). Based upon the relationship of host plant with rhizobacteria are categorized into symbiotic and free-living (Khan, 2005a,b), which gets associated either intracellularly or extracellularly. PGPRs are known to act as biofertilizers, biopesticides, phytostimulators, and rhizoremediators (Somers et al., 2004). Furthermore, research has also shown that single isolate can have more than one stimulatory action on plant growth (Kloepper, 2003). Recently, some studies have suggested that the extent of association of PGPRs varies with the plant. They can exist in extracellular (outside the plant cells/rhizosphere) or intercellular (inside the plant cell) association. Extracellular PGPRs are found to belong Agrobacterium, Arthrobacter, Bacillus cereus, Bacillus circulans, Bacillus firmus, Bacillus licheniformis, Bacillus subtilis, Enterobacter agglomerans, Enterobacter cloacae, Erwinia herbicola, Flavobacterium spp., Phyllobacterium sp., Pseudomonas aureofaciens, Pseudomonas cepacia, Pseudomonas fluorescens, Pseudomonas putida, Serratia fonticola, Serratia liquefaciens, Serratia marcescens, Serratia proteamaculans, and Bacillus thuringiensis, whereas different species of Rhizobium and Frankia showed intercellular PGPR activity (Grey and Smith, 2005). Besides these, various actinomycetes have also exhibited promising role in biocontrol of plant pathogens. The PGP compounds produced by different PGPRs are described in Table 36.1.

36.1.2 Mode of action for PGPR Enhancement in the plant growth is expected to occur due to a direct stimulation of growth via increased availability of nutrients (nitrates, nitrites, phosphorus, iron, etc.) or

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TABLE 36.1

Rhizobacteria conferring plant growth-promoting traits to plants.

Strain

Secretion

Plant

References

Enterobacter aerogenes (LJL-5), Pseudomonas aeruginosa (LJL-13)

ACC deaminase

Alfalfa

Liu et al. (2019)

Burkholderia sp. MTCC 12259

IAA, ACC deaminase

Rice

Sarkar et al. (2018)

Bacillus aryabhattai MCC3374

ACC, IAA, N2 fixation, siderophore

Rice

Ghosh et al. (2018)

Streptomyces sp. VITMS22

IAA

Mustard

Kizhakedathil (2018)

Serratia Sp.

IAA

Rauli (Nothofagus alpina)

Martı´nez et al. (2018)

Azospirillum brasilense

IAA

Soybean

Puente et al. (2017)

Azotobacter chroococcumCAZ3

IAA, siderophores, ammonia, and ACC deaminase

Maize

Rizvi and Khan (2018)

Enterobacter sp.

ACC deaminase, IAA, Siderophore, N2 fixation

Rice

Mitra et al. (2018)

E. aerogenes MCC 3092

IAA production, ACC deaminase, nitrogen fixation, and P solubilization

Rice

Pramanik et al. (2018)

Bacillus safensis

IAA, ACC deaminase

Wheat

Chakraborty et al. (2018)

Enterobacter sp. NRRU-N13, Bacillus sp. NRRU-D40

IAA

Oryza sativa L. KDML105

Saengsanga (2018)

Klebsiella pneumonia

IAA, ACC deaminase, phosphate solubilization, N2 fixation

Rice

Pramanik et al. (2017)

Enterobacter cloacae HSNJ4

IAA

Brassica napus L. (rapeseed)

Li et al. (2017)

Leifsonia xyli SE134

Gibberellins and IAA

Tomato

Kang et al. (2017)

Acinetobacter strain RSC7

IAA

Vigna radiate (mung bean)

Patel et al. (2017a,b)

E. cloacae ZNP-3

IAA production, mineral phosphate Triticum solubilization, HCN, and ammonia production aestivum (wheat)

Singh et al. (2017)

Enterobacter ludwigii PS1

Auxin, siderophore, HCN

Sea buckthorn

Dolkar et al. (2018)

Stenotrophomonas maltophilia SBP-9

ACC deaminase, gibberellic acid, IAA, siderophore, and inorganic phosphate solubilization

T. aestivum (wheat)

Singh and Jha (2017)

Bacillusspp, Alcaligenesspp, Proteus sp., and Aneurinibacillus aneurinilyticus

IAA, siderophore

Commiphora wightii

Patel et al. (2017a,b)

Pantoea sp. and Enterococcus sp.

P-solubilization ability, IAA, and siderophore

(Mung bean) V. radiata L.

Panwar et al. (2016)

(Continued)

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36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

TABLE 36.1 (Continued) Strain

Secretion

Plant

References

Arthrobacter globiformis

Siderophore

Dichanthium annulatum

Sharma et al. (2016)

Bacillus cereus

IAA, siderophore, and ACC deaminase

(Oilseed rape) B. napus L.

Etesami and Alikhani (2016)

Pseudomonas sp. PPR8

IAA, phosphate solubilization, siderophore, and ACC deaminase

Phaseolus vulgaris L.

Kumar et al. (2016)

Pseudomonas putida

Phosphate solubilization and IAA production

Mentha piperita (peppermint)

Santoro et al. (2015)

Bacillus circulans CB7

IAA, phosphate solubilization, siderophore, and ACC deaminase, nitrogenase activity

Solanum lycopersicum (tomato)

Mehta et al. (2015)

E. cloacae CAL3

IAA, ACC deaminase

Cotton plant

Mayak et al. (2001)

HCN, Hydrogen cyanide.

FIGURE 36.1 Represents plant rhizobacteria synergy favoring growth via different direct or indirect mode and action.

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36.2 Direct mechanism

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regulation of phytohormones level, or indirect mechanism of elimination of biotic stress present in the rhizosphere (Glick 2012) (Fig. 36.1).

36.2 Direct mechanism 36.2.1 N2 fixation Nitrogen occurs as the diatomic molecule. Despite being abundantly present in the atmosphere, it is not available to plants in this form for utilization into various biological processes. The atmospheric nitrogen is first reduced into the biologically active form (NH3) by microorganisms in the process of nitrogen fixation using well-established system of nitrogenase enzymes (Kim and Rees, 1994). Nitrogen fixation by microbes is an economical and environmentally sustainable process and accounts for twice the nitrogen fixed chemically in industries (Rubio and Ludden, 2008). Nitrogen-fixing bacteria either occur in symbiotic or nonsymbiotic association with plants. Symbiotic bacteria can form an association with leguminous plants (rhizobia) or nonleguminous trees (Frankia), whereas nonsymbiotic endophytes are freeliving and include cyanobacteria, Azospirillum, Azotobacter, Gluconoacetobacter, and Azoarcus, etc. (Bhattacharya and Jha, 2012). Initiation of the symbiotic relationship between rhizobia and host plant involves their complex interaction to form nodules (inhabited with intercellular rhizobia). N2 fixation is performed using nitrogenase complex, which is consist of dinitrogenase reductase and dintrogenase metalloenzyme (Dean and Jacobson, 1992). Dinitrogenase uses the electron source provided by dinitrogenase reductase to convert N2 into NH3. Dinitrogenase can have Mo, V, and Fe at its active site, but Mo is found as a metal cofactor in most of the organisms (Bishop and Joerger, 1990). Nitrogenase (nif) genes are responsible for the N2-fixing ability of microbes and are found in both symbiotic and free-living organisms. nif genes are present as a cluster of 20 24 kb long sequence with 7 operons resulting in 20 different proteins. The nif gene system is activated under low oxygen concentration and regulated by the fix-gene system.

36.2.2 Phosphate solubilization Phosphorus (P) is an essential mineral for the growth of plants due to its requirement in various biosynthetic pathways. P is present largely as insoluble, inorganic or organic compounds in the soil. The soluble forms (H2PO4 and HPO4) are available only in low concentration, which limits the plant growth. Phosphate solubilizing bacteria (PSBs) of rhizosphere support plant growth by making P available to plants. The insoluble organic phosphate is mineralized by the action of enzyme phosphatases produced by microbes, whereas inorganic phosphorus is utilized after the action of lowmolecular-weight organic acids secreted by the PSB (Zaidi et al., 2009; Glick, 2012). PSBs are common in most rhizospheric microflora, but their high sensitivity toward the environmental stress limits their application in enhancing the plant growth (Ahemad and khan, 2012a,e). It is also reported that in addition to solubilize P, PSB also enhances the

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36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

process of biological nitrogen fixation and availability of other elements (Suman et al., 2001; Zaidi et al., 2009).

36.2.3 Siderophore production Iron is a micronutrient of plant and is essential for the various physiological processes occurring in both microbes and plants. In the aerobic condition of atmosphere, iron exists as Fe31, which makes insoluble compounds that are inaccessible for plant and microbes (Rajkumar et al., 2005). Microbes sequester the extracellular iron using chelators, which are of low-molecular weight called siderophores. These are water soluble and have a high association constant for iron chelation. Siderophore produced by the microbes can be extracellular or intercellular based on their site of action. Extracellular siderophores that can only be utilized by the rhizobacteria of same genus are called homologous siderophores, whereas others that have intergenus utilization are known as heterologous siderophores. Fe31 chelated with siderophore is reduced into Fe21 on the membrane of the cell and later transported into the cell with the help of a gating mechanism. After the reduction of Fe31, siderophore can be used to chelate other ions or degraded by the cell (Rajkumar et al., 2010; Neilands, 1995). Besides their affinity for Fe31, siderophore is known to chelate with metals such as Al, Cu, Cd, Ga, In, and Pb, which have the phytotoxic effect. Formation of heavy metal siderophore complex reduces the availability of toxic-free metal ions and helps mitigate heavy metal stress in the soil. Plant makes use of different mechanisms to assimilate iron from microbial siderophore. They may directly release iron from Fe siderophore complex, uptake complete complex into the cell, or replace the ligands in the complex (Schmidt, 1999). Till now, a large number of studies have shown enhancement in plant growth with the aid of siderophore-producing rhizobacteria.

36.2.4 Phytohormone production Bacterial diversity persisting in the rhizosphere is found to actively synthesize and secrete most common auxin, IAA. IAA is known to be a crucial signaling molecule in cell division, elongation, and differentiation regulating plant growth and development (Santner et al., 2009). Furthermore, IAA has also shown its role in plants response to biotic or abiotic stresses. Besides its significance for plants, IAA has also shown to cause an alteration in several microorganisms. Therefore the role of IAA in the interaction of plant rhizobacteria seems to be very prominent. The exogenous IAA secreted by rhizobacteria intervenes with plant development by changing the pattern of endogenous IAA accumulation in different tissues (Glick, 2012; Spaepen et al., 2007). At the physiological concentration of IAA, bacterial IAA may have constitutive, destructive, or no response on the growth (Spaepen and Vanderleyden, 2011). IAA secreted by PGPR can cause an increase in the length, surface area, and biomass of root, which facilitates the nutrient availability (Llorente et al., 2016). IAA production is stimulated by tryptophan that acts as a precursor in IAA biosynthesis, but as a precursor for tryptophan anthranilate acts as an inhibitor (Zaidi et al., 2009; Spaepen et al., 2007). Tryptophan indirectly induces the IAA biosynthesis by inhibiting the activity of anthranilate synthase in negative feedback inhibition. trp genes encode the

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36.3 Indirect mechanism

867

enzymes involved in a five-step pathway for the tryptophan biosynthesis. Biosynthesis of IAA from tryptophan follows almost similar pathway in both plants and bacteria with an exception for some intermediates (Patten and Glick, 1996). IAA synthesis in plants and rhizobacteria has been identified to follow five different pathways. Indole-3-pyruvic acid and IAA mediated synthesis is majorly present in bacteria such as saprophytic Agrobacterium and Pseudomonas, Rhizobium, Azospirillum, Bradyrhizobium, Klebsiella, and Enterobacter. Certain species of Pseudomonas and Azospirilla have shown IAA formation from tryptophan with tryptamine as an intermediate. Indole-3-acetamide-mediated IAA biosynthesis is found to be active in pathogenic bacteria such as Agrobacterium tumefaciens, Pseudomonas syringae. IAA biosynthesis in Synechocystis sp. occurs with indole-3-acetonitrile formation as an intermediate. Tryptophan-independent IAA biosynthesis is mostly found in plants but also reported in rhizobacteria belonging to cyanobacteria and Azospirilla. From precursor indole-3-acetonitrile (IAN), Variovorax boronicumulans strain CGMCC 4969 can metabolize IAA, thus forming a link between plant and microbe and helps in regulation of IAA level (Sun et al., 2018). Many PGPRs have also characterized for their ability to produce cytokinins and gibberellins, but their mode of action and microbial biosynthesis pathway is not well understood (Gupta et al., 2015). PGPR-secreted gibberellins enhance the growth of the shoot, whereas cytokinins increase the root exudation, which helps to strengthen the plant microbe interaction (Ruzzi and Aroca, 2015).

36.2.5 ACC deaminase production Ethylene is a plant growth regulator and is endogenously produced for different physiological processes. Abiotic stress tends to stimulate the production of ethylene. Salinity, waterlogging, drought, heavy metal toxicity, and pathogenic microbes trigger the production of ethylene, which negatively regulates the growth of the plant (Saleem et al., 2007). PGPRs have shown to produce 1-aminocyclopropane-1-carboxylate deaminase, which reduces the level of ethylene and supports the growth, development, and tolerance to stress conditions (Nadeem et al., 2007; Zahir et al., 2008). ACC deaminase acts on the precursor of ethylene, ACC (exudated by different plant tissues), to produce ammonia and α-ketobutyrate (Honma and Shimomura, 1978). ACC deaminase-producing bacteria consequently enhances root and shoot length; nodule formation; mycorrhizal colonization; and uptake of N, P, K, and other mineral nutrients (Nadeem et al., 2007, 2010; Shaharoona et al., 2008; Glick, 2012). Rhizobacteria belonging to the genera of Acinetobacter, Achromobacter, Agrobacterium, Alcaligenes, Azospirillum, Bacillus, Burkholderia, Pseudomonas, Rhizobium, etc. have shown the characteristic of ACC deaminase production.

36.3 Indirect mechanism A wide range of microorganism has shown their application in enhancing crop production by performing as a biocontrol agent. PGPR present in the rhizosphere also indirectly accentuates the growth of plants by their activities that induce systemic pathogenic

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36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

disease resistance, competitively enhanced nutrient uptake, and antifungal and antibiotic secretion (Wang et al., 2015). PGPR secretion involves HCN, phenazines, pyrrolnitrin, 2,4diacetylphloroglucinol, pyoluteorin, viscosinamide, and tensin (Bhattacharyya and Jha, 2012). Studies based on the Arabidopsis model showed that rhizobacteria-mediated induced systemic resistance (ISR) is, independent of SA signaling cascade, triggered by jasmonic acid or/and ethylene signaling (Thomma et al., 2001). PGPRs elicit the plant response to the pathogen with the help of compounds such as 2,3-butanediol, 2,4-diaetylphloroglucinol, lipopolysaccharides, flagella, siderophore, and other Fe-regulated compounds (Maurhofer et al., 1994; Weller et al., 2004; Ryu et al., 2004; Leeman et al., 1996).

36.3.1 Root exudation strengthens synergy with rhizobacteria Root exudation causes the release of certain compounds from the root that can either attract or repel microbial community of the soil. These compounds get exposed to harmful as well as beneficiary MOs present in soil. Root exudation facilitates beneficial MOs by providing nutrients helping them to establish in the rhizosphere (de Weert et al., 2002). Even soil structure and chemistry gets affected by root exudates, which are crucial for the survival of PGPR. Azospirillum brasilense is known to modulate pH of the rhizospheric region. However, few PGPRs are used to changing the environment, and they adapt well (Carrillo et al., 2002). Alteration in root physiology was observed on inoculation with Azospirillum that changed the pattern of exudation (Heulin et al., 1987). Release of lowmolecular-weight molecules in the rhizosphere is made by root exudation. Nutrient and other molecules support microbial diversity in the rhizospheric region compared to bulk soil. Root exudates include free oxygen, ions, enzymes, diverse carbon-based metabolites, which enhance MOs number in the rhizosphere (Bertin et al., 2003; Uren, 2000). Differences in chemotaxis to root exudates cause competition among strains that enhances root colonization (Kloepper, 1992). Organic acid release from root exudation leads to acidification of rhizosphere affecting nearby population (Dakora and Phillips, 2002). All the direct and indirect mechanisms of PGPRs to promote plant growth initiate after the establishment of their symbiotic relationship. Root exudates secreted in the rhizosphere have an important role in defining the diversity and abundance of PGPRs with their ability to mediate plant microbe interaction (Curl and Truelove, 2012). Root exudates are lowmolecular-weight compounds and involve photosynthetically derived products such as sugars (arabinose, fructose, galactose, glucose, maltose, mannose, raffinose, ribose, sucrose, xylose, etc.), amino acids (α-alanine, β-alanine, arginine, asparagine, aspartic, proline, serine, tryptophan, tyrosine, etc.), organic acid (acetic, aconitic, ascorbic, citric, lactic, pyruvic, succinic, etc.), fatty acids (linoleic, linolenic, oleic, palmitic, stearic), p-amino benzoic acid, biotin, thiamine, riboflavin, pyridoxine, and hormones (IAA) (Uren, 2000). Root exudation is facilitated by active, passive, and transporter-dependent transportation (Badri and Vivanco, 2009). Amount of root exudate secreted by plant mainly depends on the species; age; cultivar; root architecture; and physical, chemical, and biological properties of soil. In cereals, around 5% 21% of the total photosynthetic product is secreted through exudation (Flores-Vargas and O’hara, 2006). Plants such as Medicago sativa, Pisum sativum, Glycine max, Lotus japonicus, Phaseolus vulgaris, and Trifolium vulgaris have also been studied for

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their root exudates (Desbrosses et al., 2005; Herna´ndez et al., 2009; Sugiyama and Yazaki, 2012). Root exudates also influence the growth of other plant species, prevents herbivore attack and availability of inorganic nutrients in the soil (Haldar and Sengupta, 2015). The complex interaction of PGPRs and host plant takes place through the regulation of metabolic signaling and gene expression of both symbionts. In the case of Rhizobium, Nod factors and other polysaccharides present on the surface regulate symbiosis after induction of their biosynthesis by the host plant. Consequently, Nod factor results in the activation of flavonoid encoding genes and accumulation of flavonoids (el Zahar Haichar et al., 2014). Accumulated flavonoids are responsible for regulating IAA level in cortical cells and nodule development (Wasson et al., 2006; Subramanian et al., 2007).

36.3.2 Impact of nanoparticles stress over rhizobacteria Studies have proven that nanoparticle (NP) affects plant, as well as microbial community of soil and its interaction with bacteria, causes a negative effect on them by penetrating their cell wall pores, and gets accumulated within cell bodies (Hwang et al., 2012; Landa et al., 2003). PGPR belonging to Bacillus sp. is commonly found associated with the pulse. The effect of graphene oxide NPs was evaluated on rhizobacteria that showed to reduce cell viability, caused a biochemical alteration in time and concentration-dependent way, and also showed negative impact over other prevailing soil communities (Gurunathan, 2015). Rhizospheric bacterium Pseudomonas chlororaphis O6 isolated from wheat roots was found to alleviate stress imposed by CuO NPs, root-colonizing by bacterium helped the plant to protect root from negative effect caused by CuO NPs (Wright et al., 2016). In maize seed germination, nanosilica imparts a positive effect on PGPR and other bacterial population and enhances the biomass and protein content of bacterial community (Karunakaran et al., 2013). In another study, AgNPs effect over rhizospheric bacteria of Oryza sativa was evaluated that showed to damage cell wall of bacteria (Mirzajani et al., 2013). Apart from conferring negative effect, NPs also have shown to confer positive effect on rhizobacteria. Bacterium P. chlororaphis O6 is known to produce IAA through the implication of indole-3-acetamide (IAM) pathway. CuO and ZnO NPs when treated at sublethal dose variably caused impact over IAA secretion; ZnO caused negative impact, while CuO favored IAA production (Dimkpa et al., 2012). Roles of PGPR and AgNPs in reducing heavy metal toxicity were evaluated on the growth of maize under municipal wastewater irrigation. The NPs showed to supplement PGPR-mediated increase in root length and root area (Khan and Bano, 2016). Titania NPs provided an interface between Bacillus amyloliquefaciens UCMB5113 and Brassica napus that augmented their interaction by enhancing adhesion and clustering of PGPR on roots conferring protection against fungal infection (Palmqvist et al., 2015). It also enhances the overall performance of PGPR (Timmusk et al., 2018). Similarly, impact of gold NPs was evaluated using broth microdilution technique over selected PGPRs where over P. putida no changes were observed, while the positive role of GNPs was observed over P. fluorescens, B. subtilis, Paenibacillus elgii, thus GNPs can be employed as nano-fertilizers (Shukla et al., 2015).

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36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

36.3.3 Rhizospheric bacteria in abiotic stress ISR: ISR confers to plant mechanism to augment defense system in response to environmental stimulus. PGPR is known to onset the ISR in plants against various stresses thus conferring plant protection (Zehnder et al., 2001; Yan et al., 2002). ISR helps plant to fight against numerous diseases and is not fixed for a specific set of microbes (Kamal et al., 2014). The defense response against pathogenic microbe is activated with the aid of ethylene signaling. A bacterial component such as cyclic lipopeptides, lipopolysaccharides, homoserine, 2,4-diacetylphloroglucinol, and siderophores induces ISR (Berendsen et al., 2015). Rhizobacteria belonging to genera Pseudomonas and Bacillus often impart negative effects thus possess the capability to initiate ISR response (Beneduzi et al., 2012) (Fig. 36.2). Plant growing in their natural environment of soil encounters various pathogenic attacks in the course of their lifetime. This has compelled different plants to evolve with mechanisms, which can overcome the pathogenicity of soilborne pathogens. Plants system triggers innate response to pathogens after the recognition of microbe-associated molecular patterns, which are common to a wide range of pathogenic microbes (Newman et al., 2013). The continuous evolution of microbes has also equipped them with the ability to defy the innate response mechanism, which makes the systemic acquired resistance (SAR) and ISR system as the key players in the plant protection against the pathogens. Induced

FIGURE 36.2

Depicts an overview of PGP traits that support the growth of plant under abiotic stress. PGP, Plant growth promoting.

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resistance is the state of plant in which it experiences higher resistance to the pathogenic activities of microbes (Choudhary et al., 2007). Induction of SAR by pathogenic or nonpathogenic microbes results in the buildup of pathogenesis-linked proteins and salicylic acid (SA). But, rhizobacteria-induced ISR is, independent of SA, regulated by jasmonic acid and ethylene (Yan et al., 2002). ISR was first reported by Van Peer et al. (1991) in Dianthus caryophyllus against Fusarium oxysporum due to elicitation by Pseudomonas sp. WCS417. Knowledge about the potential ISR elicitors and their role is not conclusive, but it is considered that the rhizobacterial elicitors are different from the pathogenic elicitors (Ebel and Mitho¨fer, 1998). ISR elicitor seems to share common features with PAMPs in inducing nonspecific defense reactions (Go´mez-Go´mez, 2004). The phenomenon of ISR is widely studied in Arabidopsis, tobacco, tomato, bean, radish, and carnation for different rhizobacteria and their elicitors (Van Loon and Bakker, 2005). Heavy metal: Heavy metals have toxic effects over plants (Nagajyoti et al., 2010; Yadav, 2010), and PGPRs are known to reduce heavy metal-induced toxicity in plants (Burd et al., 2000). Heavy metal also hampers the microbial community of soil while PGPR is known to impart tolerance to heavy metal in plants thus enhancing crop productivity (Etesami, 2018). Various PGPs such as Bacillus sp. and Pseudomonas sp. have developed mechanism to withstand toxic heavy metals through approaches such as biosorption, mobilization, and immobilization methods, surface complexion, or via cellular compartmentalization to reduce the toxicity induced by heavy metal (Singh et al., 2018). Rhizobacteria help in detoxification of heavy metals along with releasing siderophores (Khan et al., 2009). In similar study, impact of heavy metal on plant rhizosphere was analyzed that showed to reduce microbial biomass and distribution of PGPRs, a majority of them showed to bear ability to produce IAA and siderophores that supported plant growth (Melo et al., 2011). The rhizobacteria B. cereus and Pseudomonas moraviensis were isolated from Cenchrus ciliaris, when these bacteria were applied on wheat, it showed to decrease the harmful effect of heavy metal over plants (Hassan et al., 2017). Two PGPR strain Enterobacter ludwigii and Klebsiella pneumonia conferred metal tolerance in plants growing in mercury-contaminated soil and showed an enhanced length of root and shoot along with increased dry weight of root and shoot (Gontia-Mishra et al., 2016). Similarly, P. putida conferred resistance against nickel in Arabidopsis, where plant displayed increased chlorophyll content and growth of root and shoot (Someya et al., 2007). When Zea mays were inoculated with Proteus mirabilis, it has reduced toxic effect of zinc by checking the oxidative stress induced by metal (Islam et al., 2014). Legume rhizobacteria association is well known for detoxifying heavy metals thus enhances soil quality (Checcucci et al., 2017). Heavy metal-tolerant rhizobacteria and its interaction with plants can be an approach to remediate contaminated soil, this low input means can be of much importance in increasing yield of crops as well as reclamation of contaminated soil (Mishra et al., 2017). Drought: Inoculation of plants with PGPR causes alterations in biochemical and morphological traits showcasing better tolerance to abiotic stress through induced systemic tolerance (IST). Production of ACC deaminase, IAA, antioxidant enzymes, and an onset of stress genes synergistically helps to enhance crop yield by mitigating stressful condition (Etesami and Maheshwari, 2018). The IST boosts drought tolerance capability of the plant with aid of rhizobacteria that produce ACC deaminase, exopolysaccharides

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36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

(EPS), volatile organic compound (VOCs), modifications in root architecture, regulation of antioxidant enzymes, modulation of stress genes to cope with drought stress (Vurukonda et al., 2016). Underwater stress bacterium Achromobacter piechaudii ARV8 possessing potential to produce ACC deaminase displayed to enhance dry and fresh weight in pepper and tomato seedling (Mayak et al., 2004a,b). Underwater stress condition Catharanthus roseus when supplemented with P. fluorescens showed to mitigate water stress and reduced growth inhibition caused by drought (Jaleel et al., 2007). Inoculation of sunflower with P. putida produced exopolysaccharides and made a biofilm on root surface that helped to improve soil structure and alleviated drought (Sandhya et al., 2009). Table 36.2 summarizes the plant rhizobacteria synergy under abiotic stress. TABLE 36.2 An interaction between plant and rhizobacteria under abiotic stress. Strain

Plant

PGP trait

Stress

References

Pseudomonas strains GRP3A and PRS9

Maize (Zea mays L.)

Siderophore production

Under iron deficiency

Sharma and Johri (2003)

Pseudomonas spp.

Chickpea (Cicer arietinum L.)

Siderophore production

Heavy metal

Joseph et al. (2012)

Pseudomonas

Chickpea

Siderophore production

Nickel stress

Tank and Saraf (2009)

Pseudomonas fluorescens

Tomato

Phosphate solubilization, siderophore production, ACC deaminase

Salinity

Tank and Saraf (2010)

Pseudomonas aeruginosa Pseudomonas stutzeri Acinetobacter calcoaceticus Wheat

Siderophore

Bacillus licheniformis K11

Pepper

Auxin and ACC deaminase

Drought

Lim and Kim (2013)

Pseudomonas tolaasii ACC23, P. fluorescens ACC9

Canola (Brassica napus)

ACC deaminase

Cadmium

Dell’Amico et al. (2008)

Alcaligens sp.

Rice

ACC deaminase

Salt

Bal et al. (2013)

Wheat

IAA production

Saline

Sadeghi et al. (2012)

ChaudhariBhushan et al. (2009)

IAA, siderophores

Bacillus sp. Ochrobactrum sp. Streptomyces spp.

Siderophore Pi solubilization Arthrobacter sp. and Bacillus sp.

Tomato

Phosphate solubilization

Temperature, pH, and salt stresses

Banerjee et al. (2010)

Trichoderma asperellum Q1

Cucumber

Siderophore

Salinity

Qi and Zhao (2013)

(Continued)

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36.3 Indirect mechanism

TABLE 36.2

(Continued)

Strain

Plant

PGP trait

Stress

References

Achromobacter piechaudii

Lycopersicon esculentum

ACC deaminase, ethylene production

Salinity

Mayak et al. (2004a,b)

Bacillus sp. (SKU-3) Paenibacillus sp. (SKU 11)

Wheat

EPS production

Salinity

Upadhyay et al. (2011)

Serratia sp. and Rhizobium sp.

Lettuce (Lactuca sativa L.)

Nitrogen fixation

Salinity

Han and Lee (2005)

P. fluorescens TDK1

Groundnut (Arachis hypogea)

ACC deaminase

Salinity

Saravanakumar and Samiyappan (2007)

Kluyvera ascorbate SUD165

Canola

Siderophore, ACC deaminase

Heavy metal

Burd et al. (1998)

Variovorax paradoxus

Brassica juncea L.

ACC deaminase

Heavy metal

Belimov et al. (2005)

Tomato

ACC deaminase

Heavy metal

Madhaiyan et al. (2007)

Pseudomonas sp.

Soybean

Phosphate solubilization

Heavy metal

Gupta et al. (2002)

Brevibacillus

Clover Trifolium repens

Nitrogen fixation, IAA

Heavy metal

Vivas et al. (2006)

K. ascorbate

Tomato, canola, and Indian mustard

Siderophore

Heavy metal

Burd et al. (2000)

Pseudomonas sp.

Rape (B. napus)

IAA

Heavy metal

Sheng and Xia (2006)

B. juncea

IAA, phosphate solubilization

Heavy metal

Zaidi et al. (2006)

Rhodococcus sp. Methylobacterium oryzae Burkholderia sp.

Bacillus sp. Bacillus subtilis

EPS, Exopolysaccharides; PGP, plant growth promoting.

Salt: Salinity offers a major threat to agricultural production, and climate changes are expected to increase salinity. PGPR is known to boost plant growth by producing nutrient and bioactive molecules along with phytohormones that help the plant to fight salt stress situation (Egamberdieva and Lugtenberg, 2014). The rhizosphere provides a highly competitive zone that gives endurance to bacterial strain in supporting plant growth and reducing the abiotic stress. Microbial bioinoculant could provide bioprotection to crops against abiotic stresses such as salinity, heavy metal, and drought (Dimkpa et al., 2009). The redox state of salt is manipulated by bacteria by increasing the production of antioxidant enzymes, polyamines, which enhances photosynthetic efficiency (Radhakrishnan and Baek, 2017). From the rhizospheric soil of Commiphora wightii grown under salt stress, PGPR, namely, Bacillus spp., Alcaligenes spp., Proteus sp. And Aneurinibacillus aneurinilyticus were isolated that produced IAA and siderophore supporting crop production and alleviated salinity stress (Patel et al., 2017a,b). Rhizobacteria isolated from the Sulla carnosa

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36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

alleviated salt stress by reducing oxidative stress and facilitating nutrient acquisition (Hmaeid et al., 2019). From wheat rhizosphere, exopolysaccharides (EPS)-producing Bacillus sp. (SKU-3) and Paenibacillus sp. (SKU 11) were that reduce salt stress by reducing the available Na1 for plants (Upadhyay et al., 2011). Ethylene production in the plant is hampered by salt stress, increased level of ethylene can inhibit the growth of root and shoot length subsequently decreasing holistic plant growth and development (Nadeem et al., 2010). The intermediate of ethylene cycle is ACC that acts as a precursor molecule for biosynthesis, and PGPRs produce ACC deaminase that decreases the level of ACC thus eventually reducing ethylene level (Glick, 2005). Wheat grown under salt stress showed better adaptability to stress due to isolates Klebsiella sp. SBP-8-producing ACC deaminase, which enhanced salt tolerance capability of the plant (Singh et al., 2015). Likewise, in canola P. putida UW4 bearing property of producing ACC deaminase increased plant tolerance toward salinity (Li et al., 2017). From tomato, rhizosphere bacterium A. piechaudii was isolated that conferred tolerance to saline condition by augmenting ethylene production and showing ACC deaminase activity. The bacterium also showed a positive effect on increasing weight and dry weight of tomato seedling, enhanced nutrient uptake, and promoted water use efficiency (Mayak et al., 2004a,b). In this context, Cheng et al. (2007) showed that P. putida UW4-producing ACC deaminase activity induced salt tolerance in canola plant by reducing the ethylene production.

Conclusion PGPR supports nutrient recycling and assists plant growth by an alteration in microbial biology. The advances in the area have opened new direction to mitigate abiotic stress by using PGPR as bioinoculants. Abiotic stress causes a major threat to agricultural production where PGPR can serve to impart resistance against stresses such as drought, salinity, and heavy metal. The bacteria are physiologically active in rhizosphere where they produce various compounds such as growth hormones, nutrients, biocontrol agents that augment plant growth. Apart from maintaining soil fertility, it forms a key chain in the regulation of biogeochemical cycle supporting sustainable agriculture. Rhizobacteria support plant growth and also involved in reclamation of contaminated soil. Recent trends in PGPR have a set new course for these microbes in attaining sustainable agriculture practices by maintaining soil fertility, nutrient balance, enhancing crop productivity, and developing tolerant crop. Screening and selection of appropriate PGPRs, beneficial microbial community together with interdisciplinary research can open new avenues in the development of bioinoculants and opportunities with tremendous scope. Utilizing the present leads, the domains need future research focusing on the application of these PGPRs under stressed soil and development of bioinoculant for commercial use. Use of tolerant PGPR to restore the contaminated soil is at a preliminary stage. There lies a huge potential for application of these microbes in enhancing plant growth, detoxification of heavy metals and improving crop yield. However, future development in the area of bioformulation will certainly eliminate hurdles of sustainable agriculture.

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Acknowledgment The authors are thankful to the Director, MNNIT Allahabad, for providing the necessary facilities and financial support for this work.

References Ahemad, M., Khan, M.S., 2012a. Alleviation of fungicide-induced phytotoxicity in greengram [Vigna radiata (L.) Wilczek] using fungicide-tolerant and plant growth promoting Pseudomonas strain. Saudi J. Biol. Sci. 19 (4), 451 459. Ahemad, M., Khan, M.S., 2012e. Evaluation of plant-growth-promoting activities of rhizobacterium Pseudomonas putida under herbicide stress. Ann. Microbiol. 62 (4), 1531 1540. Badri, D.V., Vivanco, J.M., 2009. Regulation and function of root exudates. Plant Cell Environ. 32 (6), 666 681. Bal, H.B., Nayak, L., Das, S., Adhya, T.K., 2013. Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil 366 (1 2), 93 105. Banerjee, S., Palit, R., Sengupta, C., Standing, D., 2010. Stress induced phosphate solubilization by ’Arthrobacter’ sp. and ’Bacillus’ sp. isolated from tomato rhizosphere. Aust. J. Crop Sci. 4 (6), 378. Baudoin, E., Benizri, E., Guckert, A., 2003. Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol. Biochem. 35 (9), 1183 1192. Belimov, A.A., Hontzeas, N., Safronova, V.I., Demchinskaya, S.V., Piluzza, G., Bullitta, S., et al., 2005. Cadmiumtolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol. Biochem. 37 (2), 241 250. Beneduzi, A., Ambrosini, A., Passaglia, L.M., 2012. Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet. Mol. Biol. 35 (4), 1044 1051. Berendsen, R.L., Pieterse, C.M., Bakker, P.A., 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17 (8), 478 486. Berendsen, R.L., Verk, M.C., Stringlis, I.A., Zamioudis, C., Tommassen, J., Pieterse, C.M., et al., 2015. Unearthing the genomes of plant-beneficial Pseudomonas model strains WCS358, WCS374 and WCS417. BMC Genomics 16 (1), 539. Bertin, C., Yang, X., Weston, L.A., 2003. The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256 (1), 67 83. Bhattacharyya, P.N., Jha, D.K., 2012. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J. Microbiol. Biotechnol. 28 (4), 1327 1350. Bishop, P.E., Joerger, R.D., 1990. Genetics and molecular biology of alternative nitrogen fixation systems. Annu. Rev. Plant Biol. 41 (1), 109 125. Bloemberg, G.V., Lugtenberg, B.J., 2001. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol. 4 (4), 343 350. Brimecombe, M.J., De Leij, F.A., Lynch, J.M., 2000. The effect of root exudates on rhizosphere microbial populations. In: Pinton, R., Varini, Z., Nannipieri, P. (Eds.), The Rhizosphere, Biochemistry and Organic Substances at the Soil Plant Interface. CRC Press, pp. 95 140. Burd, G.I., Dixon, D.G., Glick, B.R., 1998. A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl. Environ. Microbiol. 64 (10), 3663 3668. Burd, G.I., Dixon, D.G., Glick, B.R., 2000. Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can. J. Microbiol. 46 (3), 237 245. ¨ ., 2007. The effect of plant growth promoting rhizobacteria on barley ˘ Cakmakci, R., Do¨nmez, M.F., Erdogan, U seedling growth, nutrient uptake, some soil properties, and bacterial counts. Turk. J. Agric. For. 31 (3), 189 199. Carrillo, A.E., Li, C.Y., Bashan, Y., 2002. Increased acidification in the rhizosphere of cactus seedlings induced by Azospirillum brasilense. Naturwissenschaften 89 (9), 428 432. Chakraborty, U., Chakraborty, B.N., Dey, P.L., Chakraborty, A.P., 2018. Bacillus safensis from wheat rhizosphere promotes growth and ameliorates salinity stress in wheat. Indian J. Biotechnol. 17, 466 479.

Plant Life under Changing Environment

876

36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

ChaudhariBhushan, L., ChincholkarSudhir, B., RaneMakarand, R., Sarode Prashant, D., 2009. Siderophoregenic Acinetobacter calcoaceticus isolated from wheat rhizosphere with strong PGPR activity. Malaysian J. Microbiol. 5 (1), 6 12. Checcucci, A., Bazzicalupo, M., Mengoni, A., 2017. Exploiting nitrogen-fixing rhizobial symbionts genetic resources for improving phytoremediation of contaminated soils. Enhancing Cleanup of Environmental Pollutants. Springer, Cham, pp. 275 288. Cheng, Z., Park, E., Glick, B.R., 2007. 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can. J. Microbiol. 53 (7), 912 918. Choudhary, D.K., Prakash, A., Johri, B.N., 2007. Induced systemic resistance (ISR) in plants: mechanism of action. Indian J. Microbiol. 47 (4), 289 297. Curl, E.A., Truelove, B., 2012. The Rhizosphere, Vol. 15. Springer Science & Business Media. Dakora, F.D., Phillips, D.A., 2002. Root exudates as mediators of mineral acquisition in low-nutrient environments. Food Security in Nutrient-Stressed Environments: Exploiting Plants’ Genetic Capabilities. Springer, Dordrecht, pp. 201 213. de Weert, S., Vermeiren, H., Mulders, I.H., Kuiper, I., Hendrickx, N., Bloemberg, G.V., et al., 2002. Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol. Plant-Microbe Interact. 15 (11), 1173 1180. de Zelicourt, A., Al-Yousif, M., Hirt, H., 2013. Rhizosphere microbes as essential partners for plant stress tolerance. Mol. Plant 6 (2), 242 245. Dean, D.R., Jacobson, M.R., 1992. In: Stacey, G., Burris, R.H., Evans, H.J. (Eds.), Biological Nitrogen Fixation. Chapman and Hall, New York. Dell’Amico, E., Cavalca, L., Andreoni, V., 2008. Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol. Biochem. 40 (1), 74 84. Desbrosses, G.G., Kopka, J., Udvardi, M.K., 2005. Lotus japonicus metabolic profiling. Development of gas chromatography-mass spectrometry resources for the study of plant-microbe interactions. Plant Physiol. 137 (4), 1302 1318. Dimkpa, C.O., Zeng, J., McLean, J.E., Britt, D.W., Zhan, J., Anderson, A.J., 2012. Production of indole-3-acetic acid via the indole-3-acetamide pathway in the plant-beneficial bacterium Pseudomonas chlororaphis O6 is inhibited by ZnO nanoparticles but enhanced by CuO nanoparticles. Appl. Environ. Microbiol. 78 (5), 1404 1410. Dimkpa, C., Weinand, T., Asch, F., 2009. Plant rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 32 (12), 1682 1694. Dolkar, D., Dolkar, P., Angmo, S., Chaurasia, O.P., Stobdan, T., 2018. Stress tolerance and plant growth promotion potential of Enterobacter ludwigii PS1 isolated from Sea buckthorn rhizosphere. Biocatal. Agric. Biotechnol. 14, 438 443. Ebel, J., Mitho¨fer, A., 1998. Early events in the elicitation of plant defence. Planta 206 (3), 335 348. Egamberdieva, D., Lugtenberg, B., 2014. Use of plant growth-promoting rhizobacteria to alleviate salinity stress in plants, Use of Microbes for the Alleviation of Soil Stresses, vol. 1. Springer, New York, pp. 73 96. el Zahar Haichar, F., Santaella, C., Heulin, T., Achouak, W., 2014. Root exudates mediated interactions belowground. Soil Biol. Biochem. 77, 69 80. Etesami, H., 2018. Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicol. Environ. Saf. 147, 175 191. Etesami, H., Alikhani, H.A., 2016. Rhizosphere and endorhiza of oilseed rape (Brassica napus L.) plant harbor bacteria with multifaceted beneficial effects. Biol. Control 94, 11 24. Etesami, H., Maheshwari, D.K., 2018. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol. Environ. Saf. 156, 225 246. Finkel, O.M., Castrillo, G., Paredes, S.H., Gonza´lez, I.S., Dangl, J.L., 2017. Understanding and exploiting plant beneficial microbes. Curr. Opin. Plant Biol. 38, 155 163. Flores-Vargas, R.D., O’hara, G.W., 2006. Isolation and characterization of rhizosphere bacteria with potential for biological control of weeds in vineyards. Journal of applied microbiology 100 (5), 946 954. Garcı´a de Salamone, I.E., Hynes, R.K., Nelson, L.M., 2001. Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Canadian Journal of microbiology 47 (5), 404 411. Ghosh, P.K., Maiti, T.K., Pramanik, K., Ghosh, S.K., Mitra, S., De, T.K., 2018. The role of arsenic resistant Bacillus aryabhattai MCC3374 in promotion of rice seedlings growth and alleviation of arsenic phytotoxicity. Chemosphere 211, 407 419.

Plant Life under Changing Environment

References

877

Glick, B.R., 2005. Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol. Lett. 251 (1), 1 7. Glick, B.R., 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012, 963401. Go´mez-Go´mez, L., 2004. Plant perception systems for pathogen recognition and defence. Mol. Immunol. 41 (11), 1055 1062. Gontia-Mishra, I., Sapre, S., Sharma, A., Tiwari, S., 2016. Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growth-promoting rhizobacteria. J. Plant Growth Regul. 35 (4), 1000 1012. Gupta, A., Gopal, M., 2008. Siderophore production by plant growth promoting rhizobacteria. Indian Journal of Agricultural Research 42 (2), 153 156. Gupta, A., Meyer, J.M., Goel, R., 2002. Development of heavy metal-resistant mutants of phosphate solubilizing Pseudomonas sp. NBRI 4014 and their characterization. Curr. Microbiol. 45 (5), 323 327. Gupta, G., Parihar, S.S., Ahirwar, N.K., Snehi, S.K., Singh, V., 2015. Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J. Microb. Biochem. Technol. 7 (2), 096 102. Gurunathan, S., 2015. Cytotoxicity of graphene oxide nanoparticles on plant growth promoting rhizobacteria. J. Ind. Eng. Chem. 32, 282 291. Hafeez, F.Y., Safdar, M.E., Chaudhry, A.U., Malik, K.A., 2004. Rhizobial inoculation improves seedling emergence, nutrient uptake and growth of cotton. Aust. J. Exp. Agric. 44 (6), 617 622. Haldar, S., Sengupta, S., 2015. Plant-microbe cross-talk in the rhizosphere: insight and biotechnological potential. Open Microbiol. J. 9, 1. Han, H.S., Lee, K.D., 2005. Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res. J. Agric. Biol. Sci. 1 (3), 210 215. Hassan, T.U., Bano, A., Naz, I., 2017. Alleviation of heavy metals toxicity by the application of plant growth promoting rhizobacteria and effects on wheat grown in saline sodic field. Int. J. Phytorem. 19 (6), 522 529. Herna´ndez, G., Valde´s-Lo´pez, O., Ramı´rez, M., Goffard, N., Weiller, G., Aparicio-Fabre, R., et al., 2009. Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiol. 151 (3), 1221 1238. Heulin, T., Guckert, A., Balandreau, J., 1987. Stimulation of root exudation of rice seedlings by Azospirillum strains: carbon budget under gnotobiotic conditions. Biol. Fertil. Soils 4 (1 2), 9 14. Hmaeid, N., Wali, M., Mahmoud, O.M.B., Pueyo, J.J., Ghnaya, T., Abdelly, C., 2019. Efficient rhizobacteria promote growth and alleviate NaCl-induced stress in the plant species Sulla carnosa. Appl. Soil Ecol. 133, 104 113. Honma, M., Shimomura, T., 1978. Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric. Biol. Chem. 42 (10), 1825 1831. Hwang, G., Ahn, I.S., Mhin, B.J., Kim, J.Y., 2012. Adhesion of nano-sized particles to the surface of bacteria: mechanistic study with the extended DLVO theory. Colloids Surf., B: Biointerfaces 97, 138 144. Islam, F., Yasmeen, T., Riaz, M., Arif, M.S., Ali, S., Raza, S.H., 2014. Proteus mirabilis alleviates zinc toxicity by preventing oxidative stress in maize (Zea mays) plants. Ecotoxicol. Environ. Saf. 110, 143 152. Jaleel, C.A., Manivannan, P., Sankar, B., Kishorekumar, A., Gopi, R., Somasundaram, R., et al., 2007. Pseudomonas fluorescens enhances biomass yield and ajmalicine production in Catharanthus roseus under water deficit stress. Colloids Surf., B: Biointerfaces 60 (1), 7 11. Joo, J.H., Yoo, H.J., Hwang, I., Lee, J.S., Nam, K.H., Bae, Y.S., 2005. Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. Febs Letters. 579 (5), 1243 1248. Joseph, B., Ranjan Patra, R., Lawrence, R., 2012. Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). Int. J. Plant Prod. 1 (2), 141 152. Kamal, R., Gusain, Y.S., Kumar, V., 2014. Interaction and symbiosis of AM fungi, actinomycetes and plant growth promoting rhizobacteria with plants: strategies for the improvement of plants health and defense system. Int. J. Curr. Microbiol. App. Sci. 3 (7), 564 585. Kang, S.M., Waqas, M., Hamayun, M., Asaf, S., Khan, A.L., Kim, A.Y., et al., 2017. Gibberellins and indole-3-acetic acid producing rhizospheric bacterium Leifsonia xyli SE134 mitigates the adverse effects of copper-mediated stress on tomato. J. Plant Interact. 12 (1), 373 380. Karunakaran, G., Suriyaprabha, R., Manivasakan, P., Yuvakkumar, R., Rajendran, V., Prabu, P., et al., 2013. Effect of nanosilica and silicon sources on plant growth promoting rhizobacteria, soil nutrients and maize seed germination. IET Nanobiotechnol. 7 (3), 70 77.

Plant Life under Changing Environment

878

36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

Kennedy, A.C., 1998. The rhizosphere and spermosphere. Principles and Applications of Soil Microbiology. Prentice-Hall, pp. 389 407. Khan, A.G., 2005a. Mycorrhizas and phytoremediation. Method in Biotechnology-Phytoremediation: Methods and Reviews. Humana Press, Totowa. Khan, A.G., 2005b. Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J. Trace Elem. Med. Biol. 18 (4), 355 364. Khan, N., Bano, A., 2016. Role of plant growth promoting rhizobacteria and Ag-nano particle in the bioremediation of heavy metals and maize growth under municipal wastewater irrigation. Int. J. Phytorem. 18 (3), 211 221. Khan, M.S., Zaidi, A., Wani, P.A., Oves, M., 2009. Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ. Chem. Lett. 7 (1), 1 19. Kim, J., Rees, D.C., 1994. Nitrogenase and biological nitrogen fixation. Biochemistry 33 (2), 389 397. Kizhakedathil, M.P.J., 2018. Rhizoshpheric bacteria isolated from the agricultural fields of Kolathur, Tamilnadu promotes plant growth in mustard plants. Biocatal. Agric. Biotechnol. 16, 293 302. Kloepper, J.W., 1978. Plant growth-promoting rhizobacteria on radishes. In: Proc. of the Fourth Internet. Conf. on Plant Pathogenic Bacter, Station de PathologieVegetale et Phytobacteriologie, vol. 2. INRA, Angers, France, 1978, pp. 879 882. Kloepper, J.W., 1992. Plant growth-promoting rhizobacteria as biological control agents. Soil Microbial Ecol. Appl. Agric. Environ.Manage. Marcel Dekker, pp. 255 274. Kloepper, J.W., 1994. Plant growth-promoting rhizobacteria (other systems). Azospirillum/Plant Associations 187, CRC Press, 137 166. Kloepper, J.W., 2003. A review of mechanisms for plant growth promotion by PGPR. In: Sixth International PGPR Workshop, vol. 10. October 2003, pp. 5 10. Kumar, P., Dubey, R.C., Maheshwari, D.K., Park, Y.H., Bajpai, V.K., 2016. Isolation of plant growth-promoting Pseudomonas sp. PPR8 from the rhizosphere of Phaseolus vulgaris L. Arch. Biol. Sci. 68 (2), 363 374. Landa, B.B., Mavrodi, D.M., Thomashow, L.S., Weller, D.M., 2003. Interactions between strains of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens in the rhizosphere of wheat. Phytopathology 93 (8), 982 994. Landa, B.B., Navas-Corte´s, J.A., Jime´nez-Dı´az, R.M., 2004. Influence of temperature on plant rhizobacteria interactions related to biocontrol potential for suppression of fusarium wilt of chickpea. Plant Pathol. 53 (3), 341 352. Leeman, M., Den Ouden, F.M., Van Pelt, J.A., Dirkx, F.P.M., Steijl, H., Bakker, P.A.H.M., et al., 1996. Iron availability affects induction of systemic resistance to Fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology 86 (2), 149 155. Li, H., Lei, P., Pang, X., Li, S., Xu, H., Xu, Z., et al., 2017. Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Appl. Soil Ecol. 119, 26 34. Lim, J.H., Kim, S.D., 2013. Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol. J. 29 (2), 201. Liu, J., Tang, L., Gao, H., Zhang, M., Guo, C., 2019. Enhancement of alfalfa yield and quality by plant growth-promoting rhizobacteria under saline-alkali conditions. J. Sci. Food Agric. 99 (1), 281 289. Llorente, B.E., Alasia, M.A., Larraburu, E.E., 2016. Biofertilization with Azospirillum brasilense improves in vitro culture of Handroanthus ochraceus, a forestry, ornamental and medicinal plant. New Biotechnol. 33 (1), 32 40. Madhaiyan, M., Poonguzhali, S., Sa, T., 2007. ). Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69 (2), 220 228. Martı´nez, O.A., Encina, C., Tomckowiack, C., Droppelmann, F., Jara, R., Maldonado, C., et al., 2018. Serratia strains isolated from the rhizosphere of raulı´ (Nothofagus alpina) in volcanic soils harbour PGPR mechanisms and promote raulı´ plantlet growth. J. Soil Sci. Plant Nutr. 18 (3), 804 819. Maurhofer, M., Hase, C., Meuwly, P., Metraux, J.P., Defago, G., 1994. Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology (USA) 84, 139 146. Mayak, S., Tirosh, T., Glick, B.R., 2001. Stimulation of the growth of tomato, pepper and mung bean plants by the plant growth-promoting bacterium Enterobacter cloacae CAL3. Biol. Agric. Hortic. 19 (3), 261 274. Mayak, S., Tirosh, T., Glick, B.R., 2004a. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 42 (6), 565 572.

Plant Life under Changing Environment

References

879

Mayak, S., Tirosh, T., Glick, B.R., 2004b. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci. 166 (2), 525 530. Mehta, P., Walia, A., Kulshrestha, S., Chauhan, A., Shirkot, C.K., 2015. Efficiency of plant growth-promoting P-solubilizing Bacillus circulans CB7 for enhancement of tomato growth under net house conditions. J. Basic Microbiol. 55 (1), 33 44. Melo, M.R., Flores, N.R., Murrieta, S.V., Tovar, A.R., Zu´n˜iga, A.G., Herna´ndez, O.F., et al., 2011. Comparative plant growth promoting traits and distribution of rhizobacteria associated with heavy metals in contaminated soils. Int. J. Environ. Sci. Technol. 8 (4), 807 816. Mirzajani, F., Askari, H., Hamzelou, S., Farzaneh, M., Ghassempour, A., 2013. Effect of silver nanoparticles on Oryza sativa L. and its rhizosphere bacteria. Ecotoxicol. Environ. Saf. 88, 48 54. Mishra, J., Singh, R., Arora, N.K., 2017. Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front. Microbiol. 8, 1706. Mitra, S., Pramanik, K., Sarkar, A., Ghosh, P.K., Soren, T., Maiti, T.K., 2018. Bioaccumulation of cadmium by Enterobacter sp. and enhancement of rice seedling growth under cadmium stress. Ecotoxicol. Environ. Saf. 156, 183 196. Mohite, B., 2013. Isolation and characterization of indole acetic acid (IAA) producing bacteria from rhizospheric soil and its effect on plant growth. Journal of soil science and plant nutrition 13 (3), 638 649. 2013. Nadeem, S.M., Zahir, Z.A., Naveed, M., Arshad, M., 2007. Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can. J. Microbiol. 53 (10), 1141 1149. Nadeem, S.M., Zahir, Z.A., Naveed, M., Asghar, H.N., Arshad, M., 2010. Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Sci. Soc. Am. J. 74 (2), 533 542. Nadeem, S.M., Ahmad, M., Zahir, Z.A., Javaid, A., Ashraf, M., 2014. The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv. 32 (2), 429 448. Nagajyoti, P.C., Lee, K.D., Sreekanth, T.V.M., 2010. Heavy metals, occurrence and toxicity for plants: a review. Environ. Chem. Lett. 8 (3), 199 216. Neilands, J.B., 1995. Siderophores: structure and function of microbial iron transport compounds. J. Biol. Chem. 270 (45), 26723 26726. Newman, M.A., Sundelin, T., Nielsen, J.T., Erbs, G., 2013. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front. Plant Sci. 4, 139. Nichols, T.D., Wolf, D.C., Rogers, H.B., Beyrouty, C.A., Reynolds, C.M., 1997. Rhizosphere microbial populations in contaminated soils. Water Air Soil Pollut. 95 (1 4), 165 178. Orhan, E., Esitken, A., Ercisli, S., Turan, M., Sahin, F., 2006. Effects of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient contents in organically growing raspberry. Scientia Horticulturae 111 (1), 38 43. Palmqvist, N.G.M., Bejai, S., Meijer, J., Seisenbaeva, G.A., Kessler, V.G., 2015. Nano titania aided clustering and adhesion of beneficial bacteria to plant roots to enhance crop growth and stress management. Sci. Rep. 5, 10146. Panwar, M., Tewari, R., Nayyar, H., 2016. Native halo-tolerant plant growth promoting rhizobacteria Enterococcus and Pantoea sp. improve seed yield of Mungbean (Vigna radiata L.) under soil salinity by reducing sodium uptake and stress injury. Physiol. Mol. Biol. Plants 22 (4), 445 459. Patel, P., Shah, R., Modi, K., 2017a. Isolation and characterization of plant growth promoting potential of Acinetobacter sp. RSC7 isolated from Saccharum officinarum cultivar Co 671. J. Exp. Biol. Agric. Sci. 5 (4), 483 491. Patel, S., Jinal, H.N., Amaresan, N., 2017b. Isolation and characterization of drought resistance bacteria for plant growth promoting properties and their effect on chilli (Capsicum annuum) seedling under salt stress. Biocatal. Agric. Biotechnol. 12, 85 89. Patten, C.L., Glick, B.R., 1996. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol. 42 (3), 207 220. Pramanik, K., Mitra, S., Sarkar, A., Soren, T., Maiti, T.K., 2017. Characterization of cadmium-resistant Klebsiella pneumoniae MCC 3091 promoted rice seedling growth by alleviating phytotoxicity of cadmium. Environ. Sci. Pollut. Res. 24 (31), 24419 24437. Pramanik, K., Mitra, S., Sarkar, A., Maiti, T.K., 2018. Alleviation of phytotoxic effects of cadmium on rice seedlings by cadmium resistant PGPR strain Enterobacter aerogenes MCC 3092. J. Hazard. Mater. 351, 317 329.

Plant Life under Changing Environment

880

36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

Puente, M.L., Gualpa, J.L., Lopez, G.A., Molina, R.M., Carletti, S.M., Cassa´n, F.D., 2017. The benefits of foliar inoculation with Azospirillum brasilense in soybean are explained by an auxin signaling model. Symbiosis 76, 41 49. Qi, W., Zhao, L., 2013. Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J. Basic Microbiol. 53 (4), 355 364. Radhakrishnan, R., Baek, K.H., 2017. Physiological and biochemical perspectives of non-salt tolerant plants during bacterial interaction against soil salinity. Plant Physiol. Biochem. 116, 116 126. Rajkumar, M., Lee, K.J., Lee, W.H., Banu, J.R., 2005. Growth of Brassica juncea under chromium stress: influence of siderophores and indole 3 acetic acid producing rhizosphere bacteria. J. Environ. Biol. 26 (4), 693 699. Rajkumar, M., Ae, N., Prasad, M.N.V., Freitas, H., 2010. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28 (3), 142 149. Rizvi, A., Khan, M.S., 2018. Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicol. Environ. Saf. 157, 9 20. Rubio, L.M., Ludden, P.W., 2008. Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annual review of microbiology 62, 93 111. Ruzzi, M., Aroca, R., 2015. Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Sci. Hortic. 196, 124 134. Ryu, C.M., Farag, M.A., Hu, C.H., Reddy, M.S., Kloepper, J.W., Pare´, P.W., 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134 (3), 1017 1026. Sadeghi, A., Karimi, E., Dahaji, P.A., Javid, M.G., Dalvand, Y., Askari, H., 2012. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J. Microbiol. Biotechnol. 28 (4), 1503 1509. Saengsanga, T., 2018. Isolation and characterization of indigenous plant growth-promoting rhizobacteria and their effects on growth at the early stage of Thai jasmine rice (Oryza sativa L. KDML105). Arabian J. Sci. Eng. 43 (7), 3359 3369. Saleem, M., Arshad, M., Hussain, S., Bhatti, A.S., 2007. Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol. 34 (10), 635 648. Sandhya, V.Z.A.S., Grover, M., Reddy, G., Venkateswarlu, B., 2009. Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol. Fertil. Soils 46 (1), 17 26. Santner, A., Calderon-Villalobos, L.I.A., Estelle, M., 2009. Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5 (5), 301. Santoro, M.V., Cappellari, L.D.R., Giordano, W., Banchio, E., 2015. Plant growth-promoting effects of native Pseudomonas strains on Mentha piperita (peppermint): an in vitro study. Plant Biol. 17 (6), 1218 1226. Saravanakumar, D., Samiyappan, R., 2007. ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J. Appl. Microbiol. 102 (5), 1283 1292. Sarkar, A., Pramanik, K., Mitra, S., Soren, T., Maiti, T.K., 2018. Enhancement of growth and salt tolerance of rice seedlings by ACC deaminase-producing Burkholderia sp. MTCC 12259. J. Plant Physiol. 231, 434 442. Schmidt, W., 1999. Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol. 141 (1), 1 26. Shaharoona, B., Naveed, M., Arshad, M., Zahir, Z.A., 2008. ). Fertilizer-dependent efficiency of pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl. Microbiol. Biotechnol. 79 (1), 147 155. Sharma, A., Johri, B.N., 2003. Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol. Res. 158 (3), 243. Sharma, M., Mishra, V., Rau, N., Sharma, R.S., 2016. Increased iron-stress resilience of maize through inoculation of siderophore-producing Arthrobacter globiformis from mine. J. Basic Microbiol. 56 (7), 719 735. Sheng, X.F., Xia, J.J., 2006. Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmiumresistant bacteria. Chemosphere 64 (6), 1036 1042. Shukla, S.K., Kumar, R., Mishra, R.K., Pandey, A., Pathak, A., Zaidi, M.G.H., et al., 2015. Prediction and validation of gold nanoparticles (GNPs) on plant growth promoting rhizobacteria (PGPR): a step toward development of nano-biofertilizers. Nanotechnol. Rev. 4 (5), 439 448.

Plant Life under Changing Environment

References

881

Singh, R.P., Jha, P.N., 2017. The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in wheat plants. Front. Microbiol. 8, 1945. Singh, R.P., Jha, P., Jha, P.N., 2015. The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J. Plant Physiol. 184, 57 67. Singh, R.P., Jha, P., Jha, P.N., 2017. ). Bio-inoculation of plant growth-promoting rhizobacterium Enterobacter cloacae ZNP-3 increased resistance against salt and temperature stresses in wheat plant (Triticum aestivum L.). J. Plant Growth Regul. 36 (3), 783 798. Singh, V.K., Singh, A.K., Singh, P.P., Kumar, A., 2018. Interaction of plant growth promoting bacteria with tomato under abiotic stress: a review. Agric. Ecosyst. Environ. 267, 129 140. Somers, E., Vanderleyden, J., Srinivasan, M., 2004. Rhizosphere bacterial signalling: a love parade beneath our feet. Crit. Rev. Microbiol. 30 (4), 205 240. Someya, N., Sato, Y., Yamaguchi, I., Hamamoto, H., Ichiman, Y., Akutsu, K., et al., 2007. Alleviation of nickel toxicity in plants by a rhizobacterium strain is not dependent on its siderophore production. Commun. Soil Sci. Plant Anal. 38 (9 10), 1155 1162. Spaepen, S., Vanderleyden, J., 2011. Auxin and plant-microbe interactions. Cold Spring Harbor Perspect. Biol. 3 (4), a001438. Spaepen, S., Vanderleyden, J., Remans, R., 2007. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31 (4), 425 448. Subramanian, S., Stacey, G., Yu, O., 2007. Distinct, crucial roles of flavonoids during legume nodulation. Trends Plant Sci. 12 (7), 282 285. Sugiyama, A., Yazaki, K., 2012. Root exudates of legume plants and their involvement in interactions with soil microbes. Secretions and Exudates in Biological Systems. Springer, Berlin, Heidelberg, pp. 27 48. Suman, A., Shasany, A.K., Singh, M., Shahi, H.N., Gaur, A., Khanuja, S.P.S., 2001. Molecular assessment of diversity among endophytic diazotrophs isolated from subtropical Indian sugarcane. World J. Microbiol. Biotechnol. 17 (1), 39 45. Sun, S.L., Yang, W.L., Fang, W.W., Zhao, Y.X., Guo, L., Dai, Y.J., 2018. The plant growth-promoting rhizobacterium Variovorax boronicumulans CGMCC 4969 regulates the level of indole-3-acetic acid synthesized from indole-3-acetonitrile. Appl. Environ. Microbiol. 84, e00298 18. Tank, N., Saraf, M., 2009. Enhancement of plant growth and decontamination of nickel-spiked soil using PGPR. J. Basic Microbiol. 49 (2), 195 204. Tank, N., Saraf, M., 2010. Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J. Plant Interact. 5 (1), 51 58. Thomma, B.P., Tierens, K.F., Penninckx, I.A., Mauch-Mani, B., Broekaert, W.F., Cammue, B.P., 2001. Different micro-organisms differentially induce Arabidopsis disease response pathways. Plant Physiol. Biochem. 39 (7 8), 673 680. Timmusk, S., Seisenbaeva, G., Behers, L., 2018. Titania (TiO2) nanoparticles enhance the performance of growthpromoting rhizobacteria. Sci. Rep. 8 (1), 617. Upadhyay, S.K., Singh, J.S., Singh, D.P., 2011. Exopolysaccharide-producing plant growth-promoting rhizobacteria under salinity condition. Pedosphere 21 (2), 214 222. Uren, N.C., 2000. Types, amounts, and possible functions of compounds released into the rhizosphere by soilgrown plants. The Rhizosphere. CRC Press, pp. 35 56. Van Loon, L.C., Bakker, P.A.H.M., 2005. Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. PGPR: Biocontrol and Biofertilization. Springer, Dordrecht, pp. 39 66. Van Peer, R., Niemann, G.J., Schippers, B., 1991. Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS 417 r. Phytopathology 81 (7), 728 734. Vivas, A., Biro, B., Ruiz-Lozano, J.M., Barea, J.M., Azcon, R., 2006. Two bacterial strains isolated from a Znpolluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere 62 (9), 1523 1533. Vurukonda, S.S.K.P., Vardharajula, S., Shrivastava, M., SkZ, A., 2016. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol. Res. 184, 13 24. Wang, X., Mavrodi, D.V., Ke, L., Mavrodi, O.V., Yang, M., Thomashow, L.S., et al., 2015. Biocontrol and plant growth-promoting activity of rhizobacteria from Chinese fields with contaminated soils. Microb. Biotechnol. 8 (3), 404 418.

Plant Life under Changing Environment

882

36. Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture

Wasson, A.P., Pellerone, F.I., Mathesius, U., 2006. Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell 18 (7), 1617 1629. Weller, D.M., Van Pelt, J.A., Mavrodi, D.V., Pieterse, C.M.J., Bakker, P.A.H.M., Van Loon, L.C., 2004. Induced systemic resistance (ISR) in Arabidopsis against Pseudomonas syringaep v. tomato by 2,4-diacetylphloroglucinol (DAPG)-producing Pseudomonas fluorescens. Phytopathology 94, S108. Weyens, N., van der Lelie, D., Taghavi, S., Newman, L., Vangronsveld, J., 2009. Exploiting plant microbe partnerships to improve biomass production and remediation. Trends Biotechnol. 27 (10), 591 598. Wright, M., Adams, J., Yang, K., McManus, P., Jacobson, A., Gade, A., et al., 2016. A root-colonizing pseudomonad lessens stress responses in wheat imposed by CuO nanoparticles. PLoS One 11 (10), e0164635. Yadav, S.K., 2010. Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S. Afr. J. Bot. 76 (2), 167 179. Yan, Z., Reddy, M.S., Ryu, C.M., McInroy, J.A., Wilson, M., Kloepper, J.W., 2002. Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92 (12), 1329 1333. Zahir, Z.A., Munir, A., Asghar, H.N., Shaharoona, B., Arshad, M., 2008. Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J. Microbiol. Biotechnol. 18 (5), 958 963. Zaidi, S., Usmani, S., Singh, B.R., Musarrat, J., 2006. Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64 (6), 991 997. Zaidi, A., Khan, M., Ahemad, M., Oves, M., 2009. Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol. Immunol. Hung. 56 (3), 263 284. Zehnder, G.W., Murphy, J.F., Sikora, E.J., Kloepper, J.W., 2001. Application of rhizobacteria for induced resistance. Eur. J. Plant Pathol. 107 (1), 39 50.

Further reading Ahemad, M., Khan, M.S., 2012b. Ecological assessment of biotoxicity of pesticides towards plant growth promoting activities of pea (Pisum sativum)-specific Rhizobium sp. strainMRP1. Emirates J. Food Agric. 24 (4), 334 343. Ahemad, M., Khan, M.S., 2012c. Effect of fungicides on plant growth promoting activities of phosphate solubilizing Pseudomonas putida isolated from mustard (Brassica compestris) rhizosphere. Chemosphere 86 (9), 945 950. Ahemad, M., Khan, M.S., 2012d. Effects of pesticides on plant growth promoting traits of Mesorhizobium strain MRC4. J. Saudi Soc. Agric. Sci. 11 (1), 63 71. Gray, E.J., Smith, D.L., 2005. Intracellular and extracellular PGPR: commonalities and distinctions in the plant bacterium signaling processes. Soil Biol. Biochem. 37 (3), 395 412. Zahir, Z.A., Ghani, U., Naveed, M., Nadeem, S.M., Asghar, H.N., 2009. Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.) under salt-stressed conditions. Arch. Microbiol. 191 (5), 415 424.

Plant Life under Changing Environment

C H A P T E R

37 Management of abiotic stress and sustainability Afaf M. Hamada1 and Youssef M. Hamada2 1

Botany and Microbiology Department, Faculty of Science, Assiut University, Assiut, Egypt 2 Water and Land Economics Researches Department, Agricultural Economics Research Institute, Agriculture Research Center, Giza, Egypt

37.1 Introduction Plants are sessile, thereby facing the changes in a surrounding medium that is oftentimes disadvantageous for outgrowth and evolution, which include (a)biotic stresses. Solely about 9% of the regions are contributory in yield output, whereas 91% are under stressors within the world (Minhas et al., 2017). Consequently, the abiotic stressors spoil a value of many millions of dollars per annum consequent to a decrease in crop output. The abiotic stress includes extreme temperatures (hot and cold), water (dryness, overflow, and drowning), light (high and low), excessive Na1 (salinity), excess or deficiency of essential nutrients, chemical factors (pH and heavy metals), air pollutants (nitrogen and sulfur dioxide and ozone), radiation (UV 100
400 nm), wind, latitude, altitude, and other stressors (Sulmon et al., 2015). Further, Fedoroff et al. (2010) reported that the negative effects of the abiotic stressors are increased through weather alteration that has been foreseen as the outcome of an increment recurrence owing to the extremist atmosphere. Abiotic stresses influence many facets of plant physiology and metabolism and can negatively impact plant outgrowth, development, and distribution. Stress responses and toleration mechanisms include the prevention or mitigation of cellular injury and restoration of growth. Abiotic stressors impact the structure, concentricity, transfer, and store of prime and subaltern metabolic products. Within restraint to abiotic stress, metabolic modulates include alteration in nitrogen and sugar metabolic pathways. Suitable activation of precocious metabolism reactions assists cell to get back biochemical and bioenergetic imbalance

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obligatory by the stressor, which is critical for adaptation. Plants have established different physiological responses to limit the effects of stress on their development. The challenge of abiotic stressors on plant outgrowth and evolution is manifested between the rising environmental effects of weather alteration (Bellard et al., 2012); therefore limitation to yield output increased with the growth being population contending for ecological sources (Wallace et al., 2003). Weather alterations are foretold to impact agrarian output the foremost, mostly at the low latitude inhabited by growing nations, together with inverse impacts of rising greenhouse emission and heat that confront research workers to invent acclimatization methods (Rosenzweig et al., 2014). That limits the universal nutrition supplies, and stable environments promote study and evolution of crops suitable for weather alteration (Wheeler and VonBraun, 2013).

37.2 Economic effects of the most disturbed abiotic stress Agrarian yield makes up a great rate of the universal markets and in several nations represents the livelihood of a human. Mahajan and Tuteja (2005) stated that due to abiotic stressors, around 50% of crop yields were reduced, making them the prime reason for crop failure worldwide. Abiotic stressors are a critical menace to sustain the agricultural industry. Recently, Rao et al. (2016) reported that naturally, a figure of stressors work with each other; thus the negative impacts are aggravated to a greater range in comparison with a single stress factor. Climate change is the prime threat to sustainable agriculture since cases of an unfavorable impact on crop yield have been confirmed. Growing human population and decreasing the availability of land for farming are duo threats to sustaining agrarian yield (Shahbaz and Ashraf, 2013). Recently, the number of people affected by nonliving stresses is massive, which explains the prevalent impacts of these proceedings (Fig. 37.1). Dryness affected a great range of the world, followed by floods and storms with very strong wind (FAO, 2011a,b). Climate, in terms of averages or events, may be an important determiner of revenue. Climate extremism is anticipated to rise worldwide, subsequently, predicting and computing the impacts on crop output are significant subjects that extend between food security and the economic vitality of crop production. A recent IPCC statement, supporting Field et al. (2012) and Porter et al. (2014) results, concerns rise in dependability to the prospect, which extremist climate proceedings can decrease nutrition producing. It has been reported (Meehl et al., 2000; Rosenzweig et al., 2001; Olesen et al., 2007; Urban et al., 2012; Min et al., 2011; Lobell et al., 2013) that the extremist proceeding is predicted to affect the volatility of harvest and is predicted as the principal menace to universal crop output.

37.3 Drought It has been stated (Ashraf 1994; Vinocur and Altman, 2005; Kasim et al., 2013; Vurukonda et al., 2016) that by 2050, dryness is predicted to induce a significant outgrowth problem plants for more than 50% of the cultivatable lands. Within the alteration of weather, dryness, and warmth, stress became the foremost significant restricting agent

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37.4 Temperature

Events Windstorms 26%

Drought 7%

Earthquakes /tsunamis 10% Extreme temperatur es 6%

Volcanic eruptions 1%

Death Windstorms 22% Drought 0%

Volcanic eruptions 0%

Mass movement: dry and wet (landslide, avalanches) 5%

Floods, waves, surges 42%

Footrest/scr ub fires 3% Mass movement: dry and wet (landslide, avalanches) 0%

Mass movement: dry and wet (landslide, avalanches) 1% Footrest/scr ub fires 0%

Affected people (thousands)

Drought 40%

Volcanic eruptions 0% Floods, waves, surges 37%

Damage (million US$) Drought 3%

Windstorms 16%

Footrest/scr ub fires 0%

Earthquakes /tsunamis 58%

Floods, waves, surges Extreme 7% temperatur es 12%

Extreme temperatur es 4%

Earthquakes /tsunamis 3%

Mass movement: dry and wet (landslide, avalanches) 0%

Earthquakes /tsunamis 19% Extreme temperatur es 4%

Windstorms 52%

Floods, waves, surges 19% Volcanic eruptions 0%

Footrest/scr ub fires 3%

FIGURE 37.1 Natural disturbances (2000
09): (A) events (%), (B) death rate (%), (C) thousands of people affected (%), and (D) damage (millions of US dollars) (%). Modified from the International Federation of Red Cross and Red Crescent Societies (IFRC & RCS) (2010).

to crop output and eventually food security. The shortage of downpour and varied rain manner are giving rise to the recurrent outset of dryness concerning the universe (Lobell et al., 2011). Intense dryness induces significant decrease in crop production via unfavorable effects on plant outgrowth and production (Yordanov et al., 2000; Barnabas et al., 2008). Recently, Daryanto et al. (2016) calculated the information of investigations issued from 1980
2015 to announce that wheat and maize production reduced by 21% and 40%, respectively, due to dryness on a worldwide scale (Daryanto et al., 2016).

37.4 Temperature The known cause of global weather alteration is the elevation of the Earth’s temperature that will worsen by releasing of greenhouse gas (GHG) invaders into the global Earth air. Further, Shi (2005), Deng et al. (2011), and Liu and Yang (2012) concluded that this expansion seriously menaces international food security.

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IPCC (2014) proclaimed that the heat of the Earth and sea surfaces has risen by 0.85 C through 132 years (1880
2012) and the average will increase by 0.2 C/decade from currently onward. The elevation of GHG concentration is changing into a main reason for world heating. Moreover, Lal (2004) and Friedlingstein et al. (2010) commented that, meanwhile, through the previous 250 years, CO2 and methane levels have risen by 30% and 150%, respectively. This stress decreases plant outgrowth and output over each ecological factor. In this status, Asseng et al. (2015) expressed that universal wheat output declined by raising the temperature to reach about a 6% decrease per one degree Celsius. In contrast, Challinor et al. (2014) and Fahad et al. (2017) cleared that rising temperature is useful for crop output in several cold zones of the planet, the general effects of which remain unfavorable on international food security (Challinor et al., 2014; Fahad et al., 2017). Lately, extremist temperatures were observed in Australia in 2012/13, 2013 in southwest US, 2015/16 in India, Pakistan, and different zones in the Middle East (Ghumman and Horney, 2016; Zommers et al., 2016), and once more in central Europe within summer 2017. It has been stated that the unusual hot event has probably been consequent to anthropogenic heating (Black et al., 2004; Stott et al., 2004; Rahmstorf and Coumou, 2012; Christidis et al., 2015). Moreover, a lot of studies currently boost the expectancy that because the weather persists to heat through the 21st century, the recurrence, size, and period of maximum heat calamities can rise, as can inhabitance facing it (Meehl and Tebaldi, 2004; Jones et al., 2015; Horton et al., 2016). In several zones of the planet, seasonal heating differences might lead to the warmest temperature elevation, over than the yearly average (Kodra and Ganguly, 2014; Horton et al., 2015; Argu¨eso et al., 2016) because the suggested techniques extend from ground external reactions (Miralles et al., 2014) to dynamical changes (Coumou et al., 2014). Recently, studies have manifested that excess temperature causes a straight menace to human life (Petkova et al., 2013), reduces agricultural yields (Hatfield et al., 2014), compromises ecosystems (Kurz et al., 2008; Lesk et al., 2017), deteriorates infrastructure (Coffel and Horton, 2015; Coffel et al., 2018), and reduces economic growth (Kjellstrom et al., 2009; Dunne et al., 2013). Low temperature is one of the fundamental environmental agents, which limits the geographic allocation of plants and is accountable for the main reduction in the output of crops (Busconi, 2001). Low temperature has a severe effect on growth, survival, reproduction, and distribution of plants (Huda´k and Salaj, 1999). Further, Baruah et al. (2011) declared that tolerance to low temperatures in plants may be categorized into two types, that is, chilling tolerance that is linked by temperatures above 0 C and freezing tolerance that is related to the temperature below 0 C. In moderate regions, most plant species are resistant to chilling temperatures and their freeze toleration to chilling temperatures can be enhanced on exposure to low temperatures. This process is called acclimatization (Heather et al., 2006; Xin and Browse, 2001). A low-temperature stressor also influences plant outgrowth, development, and crop yield. The damage due to low temperature is estimated to be $2 billion every year (Arun-Chinnappa et al., 2017). In several situations, cold stressors may not be the reason for yield damages; however, it may cause a reduction in quality. Furthermore, Hasanuzzaman et al. (2013) declared that low temperature impacts plants in various outgrowth phases resulting in decreasing outgrowth and

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production. In addition, Frederiks (2010) concluded that maximum cooling impact reduces the plant cover and exposes the plants to a temperature lower than 25 C, which freezes entire plants, ultimately leading to demise.

37.5 Flooding Floods are known amongst the old catastrophes that threaten human life (Ferreira, 2011). Around the globe, exposure of humans to floods have increased due to the growth in population and change in land-use manners. IPCC (2007) and Doocy et al. (2013) referred to the deleterious impacts of floods involving immediate death and disease and indirect displacements and spread of injury to plants, infrastructure, and possessions. Worldwide, floods, every year, lead to the death of thousands, cause displacements to a lot of people, and induce considerable damage to ownership and infrastructures (Table 37.1). Di Baldassarre et al. (2013) reported that, globally, about one billion individuals exist in floodplains, near to freshwater resource that supplies potable water, rich land, and water passageways. However, it has been reported that (ABI, 2003; Woodward et al., 2011; Alfieri et al., 2017) living close to floodplains increments the risk of stream floods induced by drastic climate events. Communities have evermore aimed to diminish the consequences of flooding through decreasing their intensity by a diversity of flooding alleviation amounts inclusive of the barrier, detention basin, early alert, and others. A long time ago, activities to minimize susceptibility usually happened solely when disasters hit the Earth (Wind et al., 1999; Kreibich and Thieken, 2009; Zurich, 2014; Jongman et al., 2015). Nonetheless, the condensation of the hydrological cycle caused by universal heating and rising exposure elevates outgrowing worries about future flood and its influences on economy and health. TABLE 37.1

Damages caused by recent floods around the world.

Time

Site

Damages

Economic damage (billion USD)

2014 (May)

Flood of Balkan

37 people died and 10000 were displaced

2.5

2013 (September)

Colorado state (United States)

8 people died and 6 were lost

1

2013 (June)

Uttarakhand (India)

6500 people died

45

2010 (July)

Indus Basin (Pakistan)

2000 people died and 20 million were affected

43

2010 (June-August)

Dadeldhura (Nepal)

98 people died, 8 were lost and 39000 were damaged

294.4

2007 (June)

Bangladesh

500 people died and 20 million were affected

1.06

Modified from , http://en.wikipedia.org/wiki/2013_North_India_Floods.; http://en.wikipedia.org/wiki/2010_Pakistan_Floods.; http//en.wikipedia. org/wiki/Floods_in_the_United_states:_2001%E2%80%93present . .

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In 1990 about 46 million individuals were suffering from floods worldwide (Hoozemans et al., 1993) and this figure is predicted to rise because of the rising average sea standard. Moreover, Nicholls et al. (1999) stated that the figure could increase to 60 million individuals if one meter of sea level rises without any other change occurring by 2100. In addition, Kates et al. (2006) referred that cases of the destructive effects of littoral floods cover the influences of Hurricane Katrina, which resulted in the demise of 1570 individuals in Louisiana and resulted in about $40
$50 billion bucks of financial damages. To rebuild the urban infrastructure and environment, it will take about 8
11 years (Kates et al., 2006). Lately, Galarneau et al. (2013) stated that Hurricane Sandy generated a harmful storm wave that amongst another region pummeled a part of the coast expansion from New Jersey to Rhode Island, which contributed to economic harm of over $50 billion and the death of 72 individuals. Furthermore, the Bhola Cyclone in 1970, in the Bay of Bengal, gave rise to floods and caused the death of individuals.

37.6 Salinity The start of the 21st century has distinctively faced a worldwide shortage of water sources, ecological contamination, exaggerated land, and watery saline (Shrivastava and Kumar, 2015). Soil salinization is a main agent that shares in the loss of output of cultivated soils. Globally, quite about 6% of the overall arable sector (about 800 million ha) is salt-affected (Munns and Tester, 2008; Hoang et al., 2016), and these areas are increasing, especially intensely, in irrigated lands (Fig. 37.2). The irrigated land of about 45 million ha (20% of the overall arable sector), that outputs one-third of the globe’s food, is salt-affected (Shrivastava and Kumar, 2015). Soil salinity impacts around 1 million ha in the European Union, fundamentally in countries of the Mediterranean Sea, and is the main reason for desertification. Also, Bowyer et al. (2009) reported that in the Mediterranean region, the predicted increment in irrigated regions and the rising scarcity of good quality water, land degradation related to the land’s alkalization can worsen at growing mean in the incoming decades. Salts that are soluble in water get deposited in the upper layer of soil to an utmost range, which affects the productivity of that region (Rengasamy, 2006). Though rainwater North America 2%

FIGURE 37.2

Impacted soils with salinity Africa 9%

NearEast 13%

Latin America 13%

The worldwide allocation (million ha) of impacted soils with salinity. Source: Hoang, T.M., Tran, T.N., Nguyen, T.K., Brett Williams, B., Wurm, P., Sean Bellairs, S., et al., 2016. Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy 6, 54

Asia,the Pacific,and Australia 53%

Europe 10%

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contains few salts, they can be amassed in the soil over a period of time. Also, salts can be deposited by soil imparted by wind from afar. The salt level increases in agrarian lands and irrigation water (Eudoxie and Wuddivira, 2014). Wang et al. (2003) pointed out that the increase of salinity in cultivated land leads to disastrous impacts worldwide. Stresses of the rising salinity, which give rise to hyperosmotic and hyperionic conditions can produce plant death (Dai et al., 2009). A number of factors, such as the extent of precipitation or evaporation and weathering of rocks, are accountable for causing salinity in a specific region. Deserts have high salinity because the amount of evaporation is higher than the amount of precipitation. Pimentel et al. (2004) stated that about 10 million ha per year of universal agrarian land are wasted by the cumulating of salts. Climate alteration, immoderate use of groundwater (fundamentally if nearby to the sea), growing use of low-quality water in irrigation, and the large introduction of irrigation related to intensive cultivation and poor drainage can accelerate the salinity. The cumulating of salts in the soil can be raised by a reduction in the leaching portion and insufficient leaching of the salts in the irrigation water. By 2050, around 50% of the arable world soil can be influenced by salinity (Bartels and Sunkar, 2005).

37.7 Greenhouse gas Agrarian output participates in gaseous releases connected with earth-cover alteration, takes part in about 80%
86% of overall food system emissions, with considerable regional variance (Vermeulen et al., 2012). Also, Vermeulen et al. (2012) reported that in 2008, all nutrition systems participated in about 20%
30% of universal anthropogenic GHG revivals, liberating around 10
17 Gt of CO2-equivalent gases. There are numerous chances for decreasing GHG revivals on each request and also the offer sides of the global nutrition systems (Garnett, 2011; Smith et al., 2013). Burney et al. (2010) stated that investment in crop production amelioration is amongst the foremost vital alleviation strategies. It has been evaluated that every greenback invested within agrarian production has led to 249 kg smaller CO2-equivalent releases compared to 1961 technologies, averting 13.1 Gt of CO2-equivalent releases for every year. Consequently, an index of a goal of 8 billion can be a “revenue” index, a manifestation of GHG/ton releasing output of agricultural products that are more harmonious for statistical agriculture indicator rules than an index of complete liberation of GHG from agrarian output. In addition, this is able to permit taking variation through nations under consideration. Probably, overcrowded nations in Africa, such as in subSaharan Africa, can reach double inhabitance numbers through 2050, which will not be anticipated to scale back total GHG liberations matched to the currently existing agrarian output.

37.8 Management of abiotic stress The universal agrarian systems should provide about 70% of additional nutrition because of the universal population, which will reach about 9 billion (Fischer et al., 2005; Smith and Gregory, 2013). In this case, Glick (2014) mentioned that the universal nutrition might shortly be insufficient to feed all the world’s folks due to increasing ecological injury

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and outgrowth of population. To cope with the increased demand, many marginal areas will be added to the agricultural system. A variety of methods have been used to reduce the effect of abiotic stress on plants. Hoang et al. (2016) commented that through strategies, water and soil administration pursuits have supported agrarian output of salinized, sidelined land; however, obtaining further output by this approach appears doubtful. With farmers continuing to achieve high crop output for every unit of farmed soil, they should leave these lands richer than what they received so that the new generations enjoy ample production. Tiwari et al. (2006) demonstrated that trying to leave the lands richer than before would require the adoption and use of production technologies supporting the newest research.

37.9 Breeding Historically, a prime aim of plant-breeding approach globally has been an amelioration of tolerance to abiotic stresses. However, the main challenge produces the complicated kinds of abiotic-stressors-tolerance signs, which then causes the problem in analyzing them into managed genetic factors adjustable into molecular breeding. Progresses in molecular biology and genome have had a great effect on the rapidity to distinguish and characterize the genetic area and genes connected with qualitative and quantitative signs. Ba¨nziger et al. (2006) concluded that breeding for stress tolerance is defined as an easy choice to tackle the challenge of decreasing crop output and yield failure produced from dryness and low land richness. Further, targets concerning plant-breeding programs (PBPs) are to improve varieties, which are quite adjusted in conformity to the aimed environments. Practically, all PBPs take advantage of multienvironment trials (METs) to assess the laterally advanced germplasm. Experimentation with METs of genotypes of significant traits at various places across various years within the targeted agroecology of the breeding program breeders is a target at holding a diversity of on-plantation conditions (Hohls, 2001; Cooper et al., 2014; Ertiro et al., 2017). Grain quality, resistance in conformity with the most substantial diseases and development bias altogether with the aimed medium are fundamental. Passioura (2012) and Rebetzke et al. (2012) stated that a rise in crop output is additionally significant, however, it is weak in heritability in dryness-prone medium. Venkateswarlu and Shanker (2009) reported that worldwide studies are performed to flourish strategies to overcome dryness stressors via the improvement of dryness-tolerant varieties, resource management practices, etc. Recently, studies have indicated that microorganisms additionally support flora to overcome dryness stressors.

37.10 Fertilizers Although cultivatable expanse would extend approximately by 70 million ha through the period 2005/07
50, the FAO projections suppose a yearly universal crop output outgrowth average of solely 0.8% (Alexandratos and Bruinsma, 2012). Closing the existing productivity inability and elevating the output ceiling should be the targets of sustainable

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FIGURE 37.3 Percentage of shared fertilizer products. Source: FAI (2012). Fertilizer Statistics 2011
12 and Earlier Issues. The Fertilizer Association of India, New Delhi; Chnada, T.K., Sati, K., 2014. Review of production, despatch and sale of nitrogen and phosphatic fertilizers in India during 2013
14. Indian J. Fertil. 10, 16.

agrarian production in ensuring the annual yield of the universe of the widely significant rise in crops production as quick as or quicker than the demand. During 2015
30 along with the least enlargement of agrarian production would need the output of the prime crops to augment around 1.3%
1.5% annually to ensure nutrition security. In addition, nations ought to take different measures, consequently feeding less grain to cattle or using them as biofuel, and boosting the crop output and adoption of crops of local importance. Sharma et al. (2014) stated that during the initial section of the Green Revolution, fertilizer consumption doubled from 7 kg in 1966
67 to 16 kg in 1971
72, and by the mid1980s, it stood at 50 kg. Report of FAI (2012) referred to the rate of fertilizer consumption in 2005
06 that was 100 kg/ha and in 2010
11 a record level of 146.3 kg/ha, which thereafter came down in 2012
13 to 128.3 kg/ha principally because of increase in the cost of phosphatic and potassic fertilizers after the entry of the NBS schema in 2010
11 (Fig. 37.3). FAI (2012) and Sharma et al. (2014) reported that throughout the last 3
4 decades, in most regions of India, there was a recorded intensive use of fertilizer to sustained growth. Previously, it has been proclaimed that fertilizer consumption in India skews extremely, with broad interprovincial, interstate, interdistrict, and intercrop differences. Further, the intensity has typically been higher in the northern zones by about 192.3 kg/ha and southern zones around 153.2 kg/ha and lower in the western by 84.6 kg/ha and eastern zones around 161.1 kg/ha. During the optimal agrarian cases the means of crop output are solely a section of most possible products or even of record products indeed gained, for all over crops, and the variation is principal because of abiotic stressors impacting the cultivation outgrowth, such as water, salt, wind, flood, extreme temperature stressors. Buchanan et al. (2000) and Fita et al. (2015) showed that all abiotic stressful stressors decrease crop output that may extend, for sugar beet or potato, from around 50% to 80% for sorghum or wheat.

37.11 Management of impacts of abiotic stress in southeast Mediterranean Sea Similar to agriculture, agribusiness is influenced by weather alteration; therefore agribusiness ought to be a section of the resolution of weather alteration acclimation,

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Production of sugar beets (1000 tons)

principally for smallholder farmers. The Mediterranean basin situated between South Europe (temperate
rainy) and North Africa (arid regions) and constitutes a transitional zone with various types of ecosystems (Doblas-Miranda et al., 2017). Agriculture backs the economy for rustic societies in the southern Mediterranean regions where it buffers rural poverty (Davidova et al., 2010; Fritsch et al., 2010) and boosts the social fabric of rustic regions by participating in more balanced rustic-land development. Climate change, therefore, threatens great effects on both the agricultural crop output and the rustic livelihoods, which rely on them (Knox et al., 2016). The fast and severe changes in climatic conditions within the next 100 years are predicted to result in a serious effect on the Mediterranean forests (Regato and Korakaki, 2010). Negative impacts are also predicted to be acuter in southern Europe wherever increased water deficiency and extreme climate events are visualized to decrease crop production, leading to major yield variability and a decrease in the regions appropriate for cultivating (Olesen and Bindi, 2002). Also, there are predicted to be considerable rises in the requirements of water for irrigation and energy for pumping (Rodrı´guez-Dı´az et al., 2011; Daccache et al., 2015). Climate changes have caused an elevation in sea levels. This has raised the quantity of salt in freshwater utilized in coastal fields. As a result, farmers are becoming increasingly incapable in utilizing the farms adjacent to the sea. FAO (2005) report stated that above 800 million ha of cultivated soil on Earth has been influenced by salinity, and according to universal weather-alteration scenarios, elevation of the sea level will menace agricultural yields in great regions by raising the soil salinity. Sugar beet, an industrial crop, is a glycophytic member of Chenopodiaceae, which is rated as the second source for sugar production worldwide after sugarcane and cultivated in 57 countries (Fig. 37.4). Moderate salinity could be used for sugar beets cultivated on Na-poor soils (25 mg/Na/kg soil). Thus the addition of Na positively influences sugar beet physiology and output mass (Durrant et al., 1978; Draycott and Christenson, 2003; Hajiboland et al., 2009). While under the semiarid situation, great amounts of Na are accumulated in plant tissues even under nonsaline situations (Wang et al., 2004; Tsialtas and Maslaris, 2006). Too much Na negatively impacts leaf morphology, physiology, output, and goodness of sugar beets being the main root of pollution under the semiarid cases (Koyro, 2000; Tsialtas and Maslaris, 2005, 2006; Wakeel et al., 2009). Sugar beet is 7000 6000

World sugar production

5000 4000 3000 2000 1000 0

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FIGURE 37.4 World sugar beet production countries in the world by 1000 tonnes 2018. Source: WorldAtlas (2018).

893

37.11 Management of impacts of abiotic stress in southeast Mediterranean Sea

susceptible to high salinity in the germination and seedling stages (Ghoulam et al., 2002; Kaffka and Hembree, 2004). Sadeghian and Yavari (2004) concluded that sugar beet seedling emergence was delayed by the effect of drought and salinity. In addition, Shehata et al. (2000) concluded that raising the salt concentration in growth medium brought a reduction in K absorption by plants of sugar beet and transition to shoots (Reda et al., 1980). Potassium increases the sugar content of beets and plays a significant biochemical role for sugar transfer in plants (Balba, 1968), thus attention must be paid to the economics of K response under salinity status (Saxena, 1985). Wang et al. (2013) found that K plays a major part in the activation of the enzyme, synthesis of protein, photosynthesis, osmoregulation, stomatal motion, transport of energy, phloem transfer, ion balance, and stressor resistance. Potassium application to sugar beet increased root and shoot mass, and qualitative characteristics and production of sugar (Mehrandish et al., 2013). Furthermore, Neseim et al. (2014) found that under salinity stress, spraying by K with yeast enhanced the growth of roots and white sugar, while reducing Na and α-amino N content of sugar beet plant. In Egypt, sugar crops are fundamental crops and most rapidly growing consumer staples. Sugar production depends on two main crops, sugarcane and sugar beet. Sugarcane was the prime origin of sugar output until the Egyptian Government adopted sugar beet production by 1982 (Esam, 2017). About 119,000 ha of sugarcane is cultivated in Upper Egypt which produces about 13,650 MT of sugar (Egypt Sugar Annual, 2017). The economy of south Egypt is heavily based on sugarcane production, and over 150,000 families live directly on farming it, in addition to extra commerce being built around sugar output. Sugar beet crops are cultivated in North Egypt in August and September and harvested in March, and about 205,000 ha is anticipated to rise. The predictable rise in the area is imputed to the government’s policy of encouraging farmers to grow beets over sugarcane to save water (Table 37.2). Sugar beet may need a shorter time than sugarcane, about half the period; therefore its output/time unit is greater than sugarcane.

TABLE 37.2

Production and distribution of sugar beets in Egypt.

Sugar beets

2015/16

2016/17

2017/18

USDA official

Latest estimates

USDA official

Latest estimates

USDA official

Latest estimates

Cultivated area

195

195

205

205

0

225

Harvested area

194

194

204

204

0

224

Production

8750

8750

9187

9187

0

9500

Total supply

8750

8750

9187

9187

0

9500

Use of sugar

8750

8750

9187

9187

0

9500

Use of alcohol

0

0

0

0

0

0

Total distribution

8750

8750

9187

9187

0

9500

Note: These are post estimates, not official USDA data. Modified from Egypt Sugar Annual, 2017. , https://www.fas.usda.gov/data/egypt-sugar-annual-2 . .

Plant Life under Changing Environment

894

37. Management of abiotic stress and sustainability

Ouda (2001) found that sugar beet demands less water, 1.4 m3 water/kg, whereas the output of the similar volume of sugars from sugarcane needed 4.0 m3 water/kg. Egypt relies on seed varieties imported from Germany, Denmark, The Netherlands, France, and Sweden due to requirements of seed production in low temperature and long duration of sunlight. Sugar is produced at about 160 MT/year from more than 123 countries worldwide, where 80% of the universal output is derived from sugarcane planted in the orbit areas and 20% is derived from sugar beet that is cultivated in mild weather (USDA FAS, 2012). Previously, sugar was a costly luxe material enjoyed solely by the rich, higher categories of the 15th and 16th centuries. Once the Spanish and Portuguese widened in sugarcane output to Puerto Rico, Cuba, and Brazil, it was transferred to Europe for refining. Germany developed sugar beet as a new source of sugar output in an early 19th century and the production had extended across Europe by the end of the century. It has been known that, in CE 710, sugar was transported to Egypt by Persia, and Arabia, where sugar was extracted from sugarcane in the far east, distributed it to their countries (Hassan and Nasr, 2008). The sugar industry in the Mediterranean region was initiated from Egypt, Syria, and Palestine in the early stages of the 7th century (Galloway, 1977). The first Egyptian sugar factory started in 1900 under Ismail Pasha (1863
79) as part of his program to improve his own agricultural assets in Middle and Upper Egypt in addition to supplying the main alternative crop to the then predominant cotton (Owen, 1984). Moreover, Hassan and Nasr (2008) referred to the oldest sugar mill in Al-Rawda in the El-Menia governorate (Anonymous, 1982), followed up by the establishment concerning 16 mills that manufactured raw sugar in the Khedive Ismail period in Upper Egypt, which was exported for refining in Europe. In addition, they clarified that the first factory to refine sugar was instituted in Al Hawamdia city by the name “The Egyptian refining company” in 1881. Now, in Egypt, out of 15 sugar mills (Table 37.3), 7 factories of sugarcane, 6 factories of sugar beet, and 1 factory of both sugarcane and beet; 13 among those are state-run companies and two are private beet factories (Egypt Sugar Annual, 2017). It was tricky to extend the cultivation of sugarcane crop as it needs giant amounts of water that is against Egyptian water policy. This matter has required acclimation to sugar beet. Thus Egypt has switched to sugar beet farming wherever there are recently reclaimed sandy soils, and due to its toleration to salinity and ability to produce high sugar output under saline situations and restricted water needs similar to other classical winter crops (Mekki, 2014). In Egypt the sugar industry varies across different states, whether in Africa or South America. Because the farmers cultivate sugarcane and beet in their own fields, then provide the manufactories through the supply contracts. Hassan and Nasr (2008) stated that in some African nations and also the New World nations, control systems of farms are possessed by the company, which possesses the manufactory, using instruments wide force further because of the range of the farm that could in some situations extend to thousands of hectares. Egypt was self-sufficient in sugar till 1973 and had an excess for export, but now aches of the deficiency in local production for covering the demand for sugar, because of elevation in population range and level of living despite Egypt being the second largest sugar producer in Africa (Fig. 37.5). The deficit in sugar production fell further as native production could not face request; therefore it was a necessity in late 1973 to import from abroad to close the deficit. Studies by Hassan and Nasr (2008) concluded that Egypt imports raw sugar to refine regionally wherever two mills were built to refine sugar, for the foreign Plant Life under Changing Environment

TABLE 37.3 Sugar cane and beet treatments. Crop

Factory

Sugarcane

Komobo

Farmers delivery (Million tons)

Sugar produced in 2015/16 (Million tons)

State-run/Private

1.80

1.934139

0.193055

State-run

Nagahamady

1.70

1.430488

0.143550

State-run

Kous

1.60

1.519286

0.158690

State-run

Armant

1.30

1.301056

0.137918

State-run

Edfo

1.10

1.229093

0.130620

State-run

Gerga

1.00

0.552612

0.054600

State-run

Deshna

1.00

0.757429

0.078396

State-run

Abu Korkas

0.70

0.339412

0.034451

State-run

10.20

9.063515

0.931280

Kafr El-Sheikh

1.75

1.877150

0.258154

State-run

Dakahlia

1.75

2.229482

0.313610

State-run

Fayoum

1.25

1.264634

0.179106

State-run

Nubaria

1.00

0.995333

0.144849

State-run

El-Nile

1.00

1.075312

0.151500

Private

Alexandria “Savola”

1.00

1.056726

0.145354

Private

Abu Korkas

0.55

0.592219

0.073024

State-run

8.30

9.090856

1.265597

Total Sugarcane Sugar beet

Total sugar beet

Total capacity (Million tons)

Total capacity, farmers’ delivery, and sugar produced numbers in MT and MY 2015/16. Modified from MALR’s Sugar Croup Council. (2016). MALR, Ministry of Agriculture and Land Reclamation, Council of Sugary Crops Annual Report, Egypt, Various Issues (MALR’s Sugar Croup Council).

896

37. Management of abiotic stress and sustainability

FIGURE 37.5 Egypt’s sugar production, consumption, and imports. Source: Egypt Sugar Annual (2017). , https://www. fas.usda.gov/data/egypt-sugar-annual-2 . .

and therefore the domestic product, the first in Al-Hawamdia and thereafter the second on the road between Cairo and Ismailia. Recently, sugar consumption is estimated at about 2.950 MT in 2016/17 (Egypt Sugar Annual, 2017). Egypt keeps providing refined sugar to food subsidy recipients at prices below the free market prices. Different water stress indicators rank Egypt as a country with extremist water stress. According to one index, in 2011, Egypt was classified number four (Maplecroft, 2012) amongst the world’s most water-scarce countries, and the World Bank considered Egypt among the top five countries with the highest risk of water stress (WWB, 2012). About 98% of Egypt’s freshwater arrives from the Nile; however, what is significant is that numerous Nile basin states are among the poorest countries on Earth, with quick population increase and growing levels of water stress and/or scarcity (Oestigaard, 2012). Around 85% of 55.5 billion cubic meters of Nile water is used for agriculture. Agriculture in Egypt could raise its capacity and its contribution to national income through the better distribution of water between crops, seasons, and locations (Gohar and Ward, 2011:755). To establish achieving efficiency and equity in the sugar industry in Egypt under scarcity of water and weather alteration, the connection between water use efficiency and sugar factories through planting acclimated sugar crop varieties for deficiency of water and salinity to make agribusiness the future of agriculture in southeast Mediterranean Sea. The poverty maps in various parts of Egypt appear as distinct properties and a potent correlation to the agricultural systems. This requires agricultural development strategies to aim for much fruitful utilization of water and to maximize the revenue earned from the water consumed. Energy utilized in agrarian systems is deemed as the main signal of potential growth and therefore the employment of the strategies to relieve its ecological effect is considered significant. In this status, Tzilivakis et al. (2005) reported that the techniques for producing crops that decrease insertion of energy, but preserve productivity are a significant ingredient of a potential agrarian growth system. The involvement of energy in the output of sugar beet was noted to be broadly affected by the nutrition of crop, which is specified by the kind of soil that the beet crop is planted in. Energy input, which uses the output of fertilizer industry, especially nitrogen, or the use of great amounts of livestock manure, to plant cultivation on the land with low fertility is very important. Generally, the insertion of energy is low, whereas plant production is high in the rich soil that has less N and K

Plant Life under Changing Environment

37.12 Mathematical model of future of sugar beet industry (FOSI) in North Egypt

897

input without the requirement for lime or salt. Further, Tzilivakis et al. (2005) exposed that the utilization of low tillage on sandy soil desired one of the least insertions with regard to the product of farming; therefore low tillage presents the chance of a lowering energy insertion to beet output. It has been observed that facilitating the allocation of irrigation water ameliorates farm situation for other agrarian practices are managed by land smoothing, which is applied to standardize land slope and regulate its surface (Brye et al., 2006). This raises irrigation management and simplifies agrarian mechanization. Moreover, TemIzel et al. (2012) reported that leveling permits lowering usage of water and its preservation. Maqsood and Khalil (2013) added that laser land leveling enhanced the irrigated area by 40%, limiting of salinity and waterlogging by around 42%, reduced land loss up to 60%, that minimized the application of fertilizers and pesticides and reciprocally enhanced the soil output via increasing the potency of fertilizer from 15% to 35% and facilitated seedling outgrowth.

37.12 Mathematical model of future of sugar beet industry (FOSI) in North Egypt Simulation models are recognized as useful tools in agricultural research. They can assist in matching empirical research returns across sites, extrapolating empirical place data to broad circumference, developing management testaments and decision prop systems, recognizing signs of weather alteration, thus making yield prognosis (Jones et al., 2003). The FOSI model was created to simulate experimental land leveling in guided fields to the two governorates. The first governorate was Kafr El Sheikh, which is located within the river delta of territorial division (31 060 42vN 30 560 45vE)close to the Mediterranean Sea and far from the capital of Egypt by about 134 kilometers (Fig. 37.6). About 3,172,753 people live in Kafr El-Sheikh, on a 3437 km2 area, out of which 76.9% live in rural area [Central Agency for Public Mobilization and Statistics of Egypt (CAPMAS), 2016]. The governorate has different mills, including a rice mill, a livestock forage manufactory, and a sugar beet manufactory. The second is Gharbia governorate located about 90 km north to Cairo, in the Nile delta of Lower Egypt (30.881 N 31.06 E) (Fig. 37.4). A population of 4,751,865, live on 25,400 km2 with most of the residents living in the rural area (70%). The governorate is famous for the textile industry. Sugar beet is cultivated in these two governorates that are affected by the rise of the sea level in Kafr El Sheikh (Fig. 37.7) (MALR, 2017). FOSI model is built to maximize revenue of sugar beet farms, maximize the efficiency of its factories in every governorate to give high production of sugar, maximize efficiency of its varieties for planting it in every governorate in the case of weather alteration, maximize its secondary crop in every factory to give high feed quality for animal production in its governorate, minimize its loss in farms in the case of weather alteration, maximize labor wages of cultivating this crop, minimize water uses in its planting, minimize fertilizer and energy consumption in its cultivation, and minimize CO2 emission in its cultivation. In addition, it has the flexibility of alleviating poverty systems as a prerequisite to attain efficiency and equity in sugar fields in North Egypt with the universal fiscal and weather alteration, reduces costs to be competing in the universal markets, water consumption, and GHG emission from sugar fields (Fig. 37.7). Moreover, it decreases the economic, financial risk, in addition to the analysis of the annual internal return rate of Plant Life under Changing Environment

898

37. Management of abiotic stress and sustainability

FIGURE 37.6

Locations of Egyptian governorates on the Mediterranean Seacoast map. Source: Hamada, Y.M., 2016. Energy use efficiency: a case study from South Mediterranean seacoast, Egypt. Agrotechnology 5, 3(Suppl). Available from: https://doi.org/10.4172/2168-9881.C1.022.

FIGURE 37.7 Sugar beet production in Kafr

Sugar beet production (ton/ha)

70

El-Sheikh and Gharbia governorates 2006. Source: MALR, 2017. Egyptian Ministry of Agricultural and Land Reclamation, Selected Data on Costs, Prices, and Land in Production, 2017.

60 50 40 30 20 10 0

Kafr El-Sheikh Governorate Gharbia Governorate

899

37.13 Optimal solutions

productivity of sugarcane varieties. To perform FOSI model, many procedures were pursued where the first one was the most favorable sugar-implanting pattern for every season and each governorate in the new and old soils in the northern area of Egypt, the second one was the simulation of the optimum implanting pattern in the North, and the third one was simulation of the optimum sugar cropping pattern of all governorates with the present one (2013/14
2015/16) to reallocate sugar crops acreage according to efficient use of water. In addition, to perform the FOSI model, field data aggregated from farmers was utilized. Also, the needed information was procured out of inclusive investigation of water consumption, other input to sugar farms on basic of seasons, and a comprehensive data concerning the farm project and related socioeconomic situations. The data considering the area, varieties, production, and cost of sugar beet crop was collected from the MALR (2017), while the data of water consumption was collected from the MWRI (2017). Further, the needful data of sugar cropping pattern input of the particular crop output system was collected from major sources and mutated to matching sugar cropping pattern values. Released GHG from sugar crops was determined and calculated as per unit of the energy input. All research data was typical and/or the rate of data was listed for the five successive years of 2013/14
2015/16.

37.13 Optimal solutions It will be quite helpful for the agribusiness future of sugar in the North of Egypt to follow the FOSI model. Application of this model has clarified possibilities of changing the area of each sugar beet variety on the basis of the soil type, weather, and quantity of TABLE 37.4

Area allotted for each variety of sugar beet in North Egypt. Kafr El-Sheikh varieties of sugar beet Area of old land (ha) Mean

FOSI

Area of new land (ha)

Change

%

Mean

FOSI

Change

%

10,234.98

6422.64

2 3812.3

2 37.2

248.64

122.64

2 126

6671.7

6460.44

2 211.3

2 3.2

120.96

120.96

0

Top

11,135.88

6317.22

2 4818.7

2 43.3

78.96

42.84

2 36.1

2 45.7

Halawa

10,423.56

6223.56

2 4200

2 40.3

255.78

234.36

2 21.4

2 8.4

Atos-bolee

6250.86

6250.86

0

0

118.86

286.86

168

141.3

Fareeda

6034.56

6034.14

2 0.4

0

70.14

112.14

42

59.9

Tord

5557.44

5557.44

0

0

55.44

55.44

0

0

Classic

5475.12

5475.12

0

0

15.12

15.12

0

0

Hosam

1252.44

1252.44

0

0

118.44

160.44

42

35.5

Gazelle

1083.18

1190

117.18

201.18

84

71.7

Baleeno Gloria

13973.4

12890.2

Plant Life under Changing Environment

2 50.7 0

900

37. Management of abiotic stress and sustainability

Area of old land (ha) Area of old land (ha) Mean

FOSI

Change

Area of new land (ha) %

Mean

FOSI

Change

%

Baleeno

574.98

836.640

261.7

45.5

0.00

0.000

0.0

0.0

Gloria

791.70

790.440

2 1.3

2 0.2

0.00

0.000

0.0

0.0

Top

635.88

761.880

126.0

19.8

0.00

0.000

0.0

0.0

Halawa

805.56

553.560

2 252.0

2 31.3

0.00

0.000

0.0

0.0

Atos-bolee

781.62

362.460

2 419.2

2 53.6

0.00

0.000

0.0

0.0

Fareeda

574.56

570.360

2 4.2

2 0.7

0.00

0.000

0.0

0.0

Tord

643.44

97.440

2 546.0

2 84.9

0.00

0.000

0.0

0.0

Classic

687.12

645.1

2 42.0

26

0.00

0.000

0.0

0.0

Hosam

538.44

412.440

2 126.0

2 23.4

0.00

0.000

0.0

0.0

Gazeel

243.18

1003

412

0.00

0.00

0.0

0.0

1246

Mean value of the used area from 2013/14 to 2015/16 to reallocate after application of FOSI model [Green color (light gray in print version) refers to the values that have increased and red color (dark gray in print version) refers to the values that have decreased]. Based on MALR, 2017. Egyptian Ministry of Agricultural and Land Reclamation, Selected Data on Costs, Prices, and Land in Production, 2017; ECAPMS, 2017. Egyptian Central Agency for Public Mobilization and Statistics, Selected Water Related Statistics., , http://www. msrintranet.capmas.gov.eg . ; FOSI model (2019).

TABLE 37.5 Changes of sugar beet varieties in North Egypt area, unit values and aggregate zone flow values from mean 2013/14
2015/16 to FOSI. Kafr El-Sheikh old and new land Mean

FOSI

Change

%

Gharbia old land and new land Mean

FOSI

Change

%

65.319

65.32

0.00

0.00

6.276

6.276

0.00

0.00

Soil type

0.37

0.47

0.09

24.59

0.04

0.04

0.01

19.02

Main sugar beet yield

2.46

3.68

1.22

49.46

0.30

0.46

0.16

54.46

Secondary sugar beet yield

2.093

3.198

1.10

52.78

0.198

0.290

0.09

46.66

Irrigated area of sugar beet in Egypt

48.27

58.87

10.60

21.95

4.86

5.66

0.80

16.50

6.49

9.33

2.84

43.75

0.65

0.94

0.29

44.20

Total sugar beet production cost

688.05

798.00

109.95

15.98

66.11

73.67

7.55

11.42

*Labor Wages

144.68

223.90

79.22

54.76

14.55

20.49

5.94

40.82

Draft Animals

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

67.78

105.65

37.87

55.87

6.82

8.56

1.74

25.52

Main sugar beet price Secondary sugar beet price

Machinery

(Continued)

Plant Life under Changing Environment

901

37.13 Optimal solutions

TABLE 37.5

(Continued) Kafr El-Sheikh old and new land Mean

FOSI

Change

Gharbia old land and new land

%

16.60

20.37

2.12

0.88

Fertilizers

76.21

77.66

1.45

Insecticides

16.85

30.33

3.88

FOSI

Change

%

22.71

1.67

1.86

0.19

11.26

2 1.24 2 58.47

0.21

0.08

2 0.13

2 60.33

1.90

8.28

7.77

2 0.51

2 6.19

13.47

79.96

1.70

2.02

0.32

19.02

4.84

0.95

24.59

0.39

0.46

0.07

19.02

24.47

36.70

12.24

50.01

2.46

3.30

0.84

34.20

217.46

311.04

93.6

43.04

21.87

29.89

8.0

36.65

1029.27

1334.44

305.16

29.65 125.27

157.88

32.61

26.04

Sugar beet profit

374.64

536.44

161.79

43.19

69.72

84.21

14.50

20.80

Sugar beet water consumption

417.89

303.01

2 114.88 2 27.49

40.95

29.12

2 11.83

2 28.89

42.10

37.26

2 4.84 2 11.49

3.60

3.56

2 0.05

2 1.34

2397.08

2154.92

2 242.16 2 10.10 207.06

205.92

2 1.15

2 0.55

Seeds Manure

Laser land leveling Other Expenses Rent Sugar beet revenue

Kerosene fuel Liter Energy consumption in cultivation MJ

3.77

Mean

Green color (light gray in print version) refers to the values that have increased and red color (dark gray in print version) refers to the values that have decreased. Based on MALR, 2017. Egyptian Ministry of Agricultural and Land Reclamation, Selected Data on Costs, Prices, and Land in Production, 2017; ECAPMS, 2017. Egyptian Central Agency for Public Mobilization and Statistics, Selected Water Related Statistics., http://www. msrintranet.capmas.gov.eg; FOSI model (2019).

TABLE 37.6 Changes of economic and financial values in sugar beet varieties in North Egypt zones from mean 2013/14
2015/16 to FOSI. Sugar beet varieties in Kafr El-Sheikh old and new land Mean Irrigated area of sugar beet Total sugar beet production cost Sugar beet revenue Sugar beet profit IRR Absolute risk

FOSI

65.319

Change %

Sugar beet varieties in Gharbia old land and new land Mean

65.32

0.00

2 688.05

2 798.00

109.95

15.98 2 66.11

1029.27

1334.44

305.16

29.65

374.64

536.44

161.79

0.50

0.67

0.18

20.96%

0.00

0.00

2 73.67

7.55

11.42

125.27

157.88

32.61

26.04

43.19

69.72

84.21

14.50

20.80

35.55

0.89

1.14

0.25

27.78

18.41%

6.276

Change % 0.00

16.17% 2 4.79% 2 22.87

6.276

FOSI

14.61% 2 3.80% 2 20.66

Green color (light gray in print version) refers to the values that have increased, and red color (dark gray in print version) refers to the values that have decreased. IRR, Internal rate of return. Based on MALR, 2017. Egyptian Ministry of Agricultural and Land Reclamation, Selected Data on Costs, Prices, and Land in Production, 2017; ECAPMS, 2017. Egyptian Central Agency for Public Mobilization and Statistics, Selected Water Related Statistics., , http://www. msrintranet.capmas.gov.eg . ; FOSI model (2019).

Plant Life under Changing Environment

902

37. Management of abiotic stress and sustainability

available water to increase financial gain in the farm. Cultivated area of sugar beet varieties, within the studied governorates, where optimal cropping pattern of sugar after application of FOSI model and also the present one, are depicted in Tables 37.4 and 37.5. The results of application of the FOSI model indicated that the land allotted for the cultivation of high-yielding varieties was larger than the low-yielding ones. Moreover, the application of laser land leveling reduced the water needed to average, which was less than the current condition. Economic evaluation of optimum cultivation based on suitable soil type, laser land leveling, and irrigation water in the new and old lands of North Egypt after application of FOSI model as compared with the existing condition is manifested in Table 37.6. Changes

35,000,000

Future of sugar beet industry (FOSI) in North Egypt Kafr El-Sheikh

30,000,000 Area (ha)

25,000,000 20,000,000 15,000,000 10,000,000 5,000,000 0000

Last irrigated area of sugar beet in Kafr El-Sheikh New irrigated area of sugar beet in Kafr El-Sheikh

3,500,000 3,000,000

Future of sugar-beet industry (FOSI) in North Egypt Gharbia

Area (ha)

2,500,000 2,000,000 1,500,000 1,000,000 500,000 0000

Last irrigated area of sugar beet in Gharbia New irrigated area of sugar beet in Gharbia

FIGURE 37.8 Optimum area allocation for cultivation of sugar beet varieties in North Egypt zones and new efficiency of sugar beet factory in North Egypt corresponding to FOSI from mean 2013/14 to 2015/16. Source: MALR, 2017. Egyptian Ministry of Agricultural and Land Reclamation, Selected Data on Costs, Prices, and Land in Production, 2017; ECAPMS, 2017. Egyptian Central Agency for Public Mobilization and Statistics, Selected Water Related Statistics. , http://www.msrintranet.capmas.gov.eg . ; FOSI model (2019).

Plant Life under Changing Environment

37.13 Optimal solutions

903

Future of sugar beet industry (FOSI) in North Egypt

Production (Ton/ha)

30,000

Kafr El-Sheikh

25,000 20,000 15,000 10,000 5000 0000

Last main sugar beet yield Varieties in Kafr El-Sheikh New main sugar beet yield Varieties in Kafr El-Sheikh 45,000 Production (Ton/ha)

40,000

Future of sugar beet industry (FOSI) in North Egypt Gharbia

35,000 30,000 25,000 20,000 15,000 10,000 5000 0000

Last main sugar beet yield Varieties in Gharbia New main sugar beet yield Varieties in Gharbia

FIGURE 37.9 Optimum yield allocation for cultivation of sugar beet varieties in North Egypt zones and new efficiency of sugar beet factory in North Egypt corresponding to FOSI from mean 2013/14 to 2015/16.

in the cultivated area and yields of sugar beet varieties, in the studied governorates of North Egypt, where the optimal cropping pattern of sugar after application of FOSI model and also the present one, are demonstrated in Figs. 37.8 and 37.9. The current study shows that 71.596 thousand ha were allocated for the cultivation of high-yield varieties of sugar beet in the two governorates of North Egypt after the application of the proposed model. In addition the outcomes stated that the net benefit was higher than that of the existing model for all cases. Our results declared that the sum of net benefit was 620.651 million E. P., in the case of FOSI application; however, the benefit of the present model was 444.360 million E.P. In addition, water consumption was lower in FOSI model (332.122 million m3) than the current one (458.834 million m3). Application of FOSI model increased annual internal rate of return in the studied governorates by 34.119, and also the absolute risk of optimum cultivation decreased by 22.635%

Plant Life under Changing Environment

904

37. Management of abiotic stress and sustainability

TABLE 37.7 Changes crop emission in cultivation in sugar beet varieties in North Egypt zones flow value from the mean 2013/14
2015/16 to FOSI, based on the equations of Ozkan et al. (2004), Erdal et al. (2007), Esengun et al. (2007), Bojaca and Schrevens (2010), Mobtaker et al. (2010), Mohammadi and Omid (2010), Rafiee et al. (2010), and Samavatean et al. (2011). Kafr_El Sheikh

Gharbia

Mean

FOSI

Change

%

Mean

FOSI

Change

%

N2O

0.021

0.019

2 11.486

0.498

0.002

0.002

2 1.335

0.498

SO2

0.101

0.090

2 11.486

2.403

0.009

0.009

2 1.335

2.403

CO2

101.693

90.013

2 11.49

2415.614

8.708

8.592

2 1.34

2415.614

SO3

nugatory

nugatory

nugatory

nugatory

nugatory

CO

0.032

0.029

0.768

0.003

0.003

CH

nugatory

nugatory

nugatory

nugatory

nugatory

nugatory

SPM

nugatory

nugatory

nugatory

nugatory

nugatory

nugatory

2 11.486

nugatory 2 1.335

0.768

Green color (light gray in print version) referred to the values that have increased, and red color (dark gray in print version) referred to the values that have decreased. Nitrous oxide (N2O), sulfur dioxide (SO2), carbon dioxide (CO2), sulfur trioxide (SO3), carbon monoxide (CO), methane (CH4) and suspended particulate matter (SPM). Based on Ozkan, B., Kurklu, A., Akcaoz, H., 2004. An input-output energy analysis in greenhouse vegetable production: a case study for Antalya region of Turkey. Biomass Bioenergy 26, 89
95; Erdal, G., Esengun, K., Erdal, H., Gunduz, O., 2007. Energy use and economical analysis of sugar beet production in Tokat province of Turkey. Energy 32, 35
41; Esengun, K., Gu¨ndu¨z, O., Erdal, G., 2007. Input-output energy analysis in dry apricot production of Turkey. Energy Convers. Manage. 48, 592
598; Bojaca´, C.R., Schrevens, E., 2010. Energy assessment of peri-urban horticulture and its uncertainty: case study for Bogota, Colombia. Energy 35, 2109
2118; Mobtaker, H.G., Keyhani, A., Mohammadi, A., Rafiee, S., Akram, A., 2010. Sensitivity analysis of energy inputs for barley production in Hamedan Province of Iran. Agric. Ecosyst. Environ. 137, 367
372; Mohammadi, A., Omid, M., 2010. Econometrical analysis and relation between energy inputs and yield of greenhouse cucumber production in Iran. Appl. Energy 87, 191
196; Rafiee, S., Avval, S.H.M., Mohammadi, A., 2010. Modeling and sensitivity analysis of energy inputs for apple production in Iran. Energy 35, 3301
3306; Samavatean, N., Rafiee, S., Mobli, H., Mohammadi, A., 2011. An analysis of energy use and relation between energy inputs and yield, costs and income of garlic production in Iran. Renew. Energy 36, 1808
1813; MALR, 2017. Egyptian Ministry of Agricultural and Land Reclamation, Selected Data on Costs, Prices, and Land in Production, 2017; ECAPMS, 2017. Egyptian Central Agency for Public Mobilization and Statistics, Selected Water Related Statistics. http://www.msrintranet.capmas.gov.eg; FOSI model (2019).

(Table 37.7). Consistent with the FOSI model, sugarcane factories that were operating in high efficiency reached 100% in the studied governorates. Air contamination influences the atmosphere, economy, and people’s health. Regarding GHG, the FOSI model released lower emissions as compared with the existing model for sugar beet production. Table 37.7 showed the social cost of every ton’s emission of GHG and air pollutants, which was calculated from the data of the optimal use of energy in the studied area in North Egypt. Laser land leveling cost in the studied area was low (357.142 E.P./ha), thus farmers should apply it in their fields, because the revenue will increase by 3259.524 E.P./ha and additionally save water by 27.616%. According to the application of FOSI, it was noticed that the whole cultivated area of sugar beet is going to remain as before. What is more, farm financial gain is going to be increased by 39.673%, water use can decrease by 27.616%, GHG emission can cut back by 10.684%, and energy can be reduced by 9.343%.

Plant Life under Changing Environment

References

905

References ABI, 2003. Assessment of the Cost and Effect on Future Claims of Installing Flood Damage Resistant Measures. Assoc. British Insurers, London, UK. Alexandratos, N., Bruinsma, J., 2012. World agriculture towards 2030/2050: the 2012 revision. ESA Working Paper No. 12-03. FAO, Rome, 2012. ,http://www.fao.org/docrep/016/ap106e/ap106e.pdf.. Alfieri, L., Bisselink, B., Dottori, F., Naumann, G., de Roo, A., Salamon, P., et al., 2017. Global projections of river flood risk in a warmer world. Earth’s Future 5, 171
182. Available from: https://doi.org/10.1002/2016EF000485. Anonymous, 1982. National Specialized Councils (1982) The Pillars of Strategic Industry Part II
Cairo, p. 10 (in Arabic). Argu¨eso, D., Di Luca, A., Perkins-Kirkpatrick, S.E., Evans, J.P., 2016. Seasonal mean temperature changes control future heat waves. Geophys. Res. Lett. 43, 7653
7660. Arun-Chinnappa, K.S., Ranawake, L., SamanSeneweera, S., 2017. Impacts and management of temperature and water stress in crop plants. In: Minhas, P.S. et al. (Eds.), Abiotic Stress Management for Resilient Agriculture, Springer Nature Singapore Pte Ltd, pp. 221
233. Ashraf, M., 1994. Breeding for salinity tolerance in plants. Crit. Rev. Plant Sci. 13, 17
42. Asseng, S., Ewert, F., Martre, P., Ro¨tter, R.P., Lobell, D.B., Cammarano, D., et al., 2015. Rising temperatures reduce global wheat production. Nat. Clim. Change 5, 143
147. Balba, A.M., 1968. Soil Fertility. Dar El-Matboat El-Gadida, Alex., Egypt. (In Arabic). Ba¨nziger, M., Setimela, P.S., Hodson, D., Vivek, B., 2006. Breeding for improved abiotic stress tolerance in maize adapted to southern Africa. Agric. Water Manage. 80, 212
224. Available from: https://doi.org/10.1016/j. agwat.2005.07.014. Barnabas, B., Ja¨ger, K., Fehe´r, A., 2008. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 31, 11
38. Bartels, D., Sunkar, R., 2005. Drought and salt tolerance in plants. Crit. Rev. Plant Sci. 24, 23
58. Baruah, A.R., Onishi, K., Oguma, Y., Oka, N.I., Uwatoko, N., Sano, Y., 2011. Effects of acclimation on chilling tolerance in Asian cultivated and wild rice. Euphytica 181, 293
303. Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W., Courchamp, F., 2012. Impacts of climate change on the future of biodiversity. Ecol. Lett. 15, 365
377. Black, E., Blackburn, M., Harrison, G., Hoskins, B.J., Methven, J., 2004. Factors contributing to the summer 2003 European heatwave. Weather 59, 217
223. Bojaca´, C.R., Schrevens, E., 2010. Energy assessment of peri-urban horticulture and its uncertainty: case study for Bogota, Colombia. Energy 35, 2109
2118. Bowyer, C., Withana, S., Fenn, I., Bassi, S., Lewis, M., Tamsi, C., et al., 2009. Land Degradation and Desertification: EU Policy Response and Future Priorities, 2009. European Parliament, Policy Department, Economic and Scientific Policy, ,http://www.ieep.eu/assets/431/land_degdesert.pdf. [Cited 29 April 2016]. Brye, K.R., Slaton, N.A., Norman, R.J., 2006. Soil physical and biological properties as affected by land leveling in a clayey. Aquert. Soil Sci. Soc. Am. J. 70, 631
642. Buchanan, B.B., Gruissem, W., Jones, R.L., 2000. Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD. Burney, J.A., Davis, S.J., David, B., Lobell, D.B., 2010. Greenhouse gas mitigation by agricultural intensification. Proc. Natl. Acad. Sci. U.S.A. 107, 12052
12057. Busconi, L., 2001. A rice membrane-bound calcium-dependent protein kinase is activated in response to low temperature. Plant Physiol. 125, 1442
1449. Central Agency for Public Mobilization and Statistics of Egypt (CAPMAS), Statistical Year Book for Agriculture, 2016. Challinor, A., Martre, P., Asseng, S., Thornton, P., Ewert, F., 2014. Making the most of climate impacts ensembles. Nat. Clim. Change 4, 77
80. Chnada, T.K., Sati, K., 2014. Review of Production, Despatch and Sale of Nitrogen and Phosphatic Fertilizers in India during 2013
14. Indian J. Fertil. 10, 16
21. Christidis, N., Jones, G.S., Stott, P.A., 2015. Dramatically increasing chance of extremely hot summers since the 2003 European heatwave. Nat. Clim. Change 5, 46
50. Coffel, E., Horton, R., 2015. Climate change and the impact of extreme temperatures on aviation weather. Clim. Soc. 7, 94
102.

Plant Life under Changing Environment

906

37. Management of abiotic stress and sustainability

Coffel, E.D., Horton, R.M., de Sherbinin, A., 2018. Temperature and humidity based projections of a rapid rise in global heat stress exposure during the 21st century. Environ. Res. Lett. 13, 014001. Available from: https:// doi.org/10.1088/1748-9326/aaa00e. Cooper et al. Cooper, M., Gho, C., Leafgren, R., Tang, T., Messina, C., 2014. Breeding drought-tolerant maize hybrids for the US corn-belt: discovery to product. J. Exp. Bot. 65, 6191
6204. Coumou, D., Petoukhov, V., Rahmstorf, S., Petri, S., Schellnhuber, H.J., 2014. Quasi-resonant circulation regimes and hemispheric synchronization of extreme weather in boreal summer. Proc. Natl. Acad. Sci. U.S.A. 111, 12331
12336. Daccache, A., Ciurana, J.S., Rodriguez Diaz, J.A., Knox, J.W., 2015. Water and energy footprint of irrigated agriculture in the Mediterranean region. Environ. Res. Lett. 9, 124014. Dai, Q.-L., Chen, C., Feng, B., Liu, T.-T., Tian, X., Gong, Y.-Y., et al., 2009. Effects of different NaCl concentration on the antioxidant enzymes in oilseed rape (Brassica napus L.) seedlings. Plant Growth Regul. 59, 273
278. Daryanto, S., Wang, L., Jacinthe, P.A., 2016. Global synthesis of drought effects on maize and wheat production. PLoS One 11, e0156362. Davidova, S., Gorton, M., Fredriksson, L., 2010. Semi-Subsistence Farming in Europe: Concepts and Key Issues [online document]. Available at ,http://enrd.ec.europa.eu/enrdstatic/fms/pdf/FB3C4513-AED5-E24F-E70AF7EA236BBB5A.pdf. (accessed 21.02.15.). Deng, X.Z., Lin, Y.Z., Ge, Q.S., Zhao, Y.H., 2011. Impact of drought on price fluctuation of agricultural production across the North China Region. Resour. Sci. 33, 766
772 (in Chinese). Di Baldassarre, G., Viglione, A., Carr, G., Kuil, L., Salinas, J.L., Bloschl, G., 2013. Socio-hydrology: conceptualising human-flood interactions. Hydrol. Earth Syst. Sci. 17, 3295
3303. Doblas-Miranda, E., Alonso, R., Arnan, X., Bermejo, V., Brotons, L., et al., 2017. A review of the combination among global change factors in forests, shrublands and pastures of the Mediterranean region: beyond drought effects. Global Planet. Change 148, 42
54. Doocy, S., Daniels, A., Murray, S., Kirsch, T.D., 2013. The human impact of floods: a historical review of events 1980
2009 and systematic literature review. Rev. PLoS Curr. Dis. Available from: https://doi.org/10.1371/ currents.dis.f4deb457904936b07c09daa98ee8171a. Draycott, A.P., Christenson, D.R., 2003. Nutrients for Sugar Beet Production: Soil-Plant Relationships. CABI Publishing, Wallingford, UK. Dunne, J.P., Stouffer, R.J., John, J.G., 2013. Reductions in labour capacity from heat stress under climate warming. Nat. Clim. Change 3, 563
566. Durrant, M.J., Draycott, A.P., Milford, G.F.J., 1978. Effect of sodium fertilizer on water status and quality of sugar beet. Ann. Appl. Biol. 88, 321
328. ECAPMS, 2017. Egyptian Central Agency for Public Mobilization and Statistics, Selected Water Related Statistics. ,http://www.msrintranet.capmas.gov.eg.. Egypt Sugar Annual, 2017. ,https://www.fas.usda.gov/data/egypt-sugar-annual-2.. Erdal, G., Esengun, K., Erdal, H., Gunduz, O., 2007. Energy use and economical analysis of sugar beet production in Tokat province of Turkey. Energy 32, 35
41. Ertiro, B.T., Beyene, Y., Das, B., Mugo, S., Olsen, M., Oikeh, S., et al., 2017. Combining ability and testcross performance of drought-tolerant maize inbred lines under stress and non-stress environments in Kenya. Plant Breed 136, 197
205. Esam, B.A., 2017. Economic modelling and forecasting of sugar production and consumption in Egypt. Int. J. Agric. Econ. 2, 96
109. Esengun, K., Gu¨ndu¨z, O., Erdal, G., 2007. Input
output energy analysis in dry apricot production of Turkey. Energy Convers. Manage. 48, 592
598. Eudoxie, G.D., Wuddivira, M., 2014. Soil, water, and agricultural adaptations. In: Ganpat, W.G., Isaac, W.A. (Eds.), Impacts of Climate Change on Food Security in Small Island Developing States, IGI Global, 255 pp. Fahad, S., Bajwa, A.A., Nazir, U., Anjum, S.A., Farooq, A., Zohaib, A., et al., 2017. Crop production under drought and heat stress: plant responses and management options. Front. Plant Sci. 2017 B, 1
16. FAI, 2012. Fertilizer Statistics 2011-12 and Earlier Issues. The Fertilizer Association of India, New Delhi. FAO (Food and Agriculture Organization of the United Nations), 2005. Global Network on Integrated Soil Management for Sustainable Use of Salt-Affected Soils. Land and Plant Nutrition Management Services, Rome (Italy). FAO, 2011a. Quinoa: An Ancient Crop to Contribute to World Food Security. Available at ,http://www.fao. org/fileadmin/templates/aiq2013/res/en/cultivo.quinuaen.pdf. (accessed 17.09.14.).

Plant Life under Changing Environment

References

907

FAO, 2011b. The State of Food and Agriculture. World Sugar Beet Production. Fedoroff, N.V., Battisti, D.S., Beachy, R.N., Cooper, P.J.M., Fischhoff, D.A., Hodges, C.N., et al., 2010. Radically rethinking agriculture for the 21st century. Science 327, 833
834. Ferreira, S., 2011. Nature, socio-economics and flood-mortality. In: Proceedings of the 2011 Georgia Water Resources Conference. University of Georgia, Athens, GA, April 11
13. Field, C., Barros, V., Stocker, T., Dahe, Q., Dokken, D., Ebi, K., et al., 2012. Managing the risks of extreme events and disasters to advance climate change adaptation. Special Report of the Intergovernmental Panel on Climate Change, Geneva, Switzerland. Cambridge University Press, New York. Fischer, G., Shah, M., Tubiello, F.N., VanVelhuizen, H., 2005. Socio-economic and climate change impacts on agriculture: an integrated assessment, 1990
2080. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 360, 2067
2083. Fita, A., Rodrı´guez-Burruezo, A., Boscaiu, M., Prohens, J., Vicente, O., 2015. Breeding and domesticating crops adapted to drought and salinity: a new paradigm for increasing food production. Front. Plant Sci. 6. Frederiks, T.M., 2010. Frost Resistance in Cereals After Ear Emergence (Ph.D. thesis). The University of Southern Queensland. Friedlingstein, P., Houghton, R.A., Marland, G., Hackler, J., Boden, T.A., Conway, T.J., et al., 2010. Update on CO2 emissions. Nat. Geosci. 3, 811
812 (2010). Fritsch, J., Wegener, S., Buchenrieder, G., Curtiss, J., Gomezy Paloma, S., 2010. Economic prospect for semisubsistence farm households in EU New Member States. In: JRC Technical Report, EUR 24418 EN. Galarneau, T.J., Davis, C.A., Shapiro, M.A., 2013. Intensification of Hurricane Sandy (2012) through extratropical warm core seclusion. Mon. Weather Rev. 141, 42964321. Galloway, J.H., 1977. The Mediterranean sugar industry. Geogr. Rev. 67, 177
194. Garnett, T., 2011. Where are the best opportunities for reducing greenhouse gas emissions in the food system (including the food chain)? Food Policy 36, S23
S32. Ghoulam, C., Foursy, A., Fares, K., 2002. Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ. Exp. Bot. 47, 39
50. Ghumman, U., Horney, J., 2016. Characterizing the impact of extreme heat on mortality, Karachi, Pakistan, June 2015. Prehosp. Disaster Med. 31, 263
266. Glick, B.R., 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169, 30
39. Gohar, A.A., Ward, F.A., 2011. ‘Gains from improved irrigation water use efficiency in Egypt’. Int. J. Water Resour. Dev. 27, 737
758. Hajiboland, R., Joudmand, A., Fotouhi, K., 2009. Mild salinity improves sugar beet (Beta vulgaris L.) quality. Acta Agric. Scand. Sect. B—Soil Plant Sci. 59, 295
305. Hamada, Y.M., 2016. Energy use efficiency: a case study from South Mediterranean seacoast, Egypt. Agrotechnology 5 (Suppl), 3. Available from: https://doi.org/10.4172/2168-9881.C1.022. Hamada, Y.M., 2019. FOSI, the mathematical model of the future of the sugar beet industry in North Egypt. Hasanuzzaman, M., Nahar, K., Alam, M., Roychowdhury, R., Fujita, M., 2013. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 14, 9643
9684. Available from: https://doi.org/10.3390/ijms14059643. Hassan, S.F., Nasr, M.I., 2008. Sugar industry in Egypt. Sugar Tech. 10, 204
209. Hatfield, J.L., Takle, G., Grothjahn, R., Holden, P., Izaurralde, R.C., Mader, T., et al., 2014. Ch. 6: Agriculture. In: Melillo, J.M., Richmond, T.C., Yohe, G.W. (Eds.), Climate Change Impacts in the United States: The Third National Climate Assessment, pp. 150
174. Available from: https://doi.org/10.7930/J02Z13FR. Heather, A., Van Buskirk, H.A., Thomashow, M.F., 2006. Arabidopsis transcription factors regulating cold acclimation. Physiol. Plant 126, 72
80. Hoang, T.M., Tran, T.N., Nguyen, T.K., Brett Williams, B., Wurm, P., Sean Bellairs, S., et al., 2016. Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy 6, 54. Hohls, T., 2001. Conditions under which selection for mean productivity, tolerance to environmental stress, or stability should be used to improve yield across a range of contrasting environments. Euphytica 120, 235
245. Hoozemans, F.M.J., Marchand, M., Pennekamp, H.A., 1993. A Global Vulnerability Analysis: Vulnerability Assessment for Population, Coastal Wetlands and Rice Production on a Global Scale, second ed. Delft Hydraulics, The Netherlands. Horton, R.M., Coffel, E.D., Winter, J.M., Bader, D.A., 2015. Projected changes in extreme temperature events based on the NARCCAP model suite. Geophys. Res. Lett. 42, 7722
7731.

Plant Life under Changing Environment

908

37. Management of abiotic stress and sustainability

Horton, R.M., Mankin, J.S., Lesk, C., Coffel, E., Raymond, C.A., 2016. Review of recent advances in research on extreme heat events. Curr. Clim. Change Rep. 2, 242
259. Huda´k, J., Salaj, J., 1999. The effect of low temperatures on the structure of plant cells. In: Pessarakli, M. (Ed.), Handbook of Plant and Crop Stress, second ed. Marcel Dekker, New York
Basel, pp. 441
464. International Federation of Red Cross and Red Crescent Societies (IFRC & RCS), 2010. World Disasters ReportFocus on Urban Risk. Geneva. IPCC, 2007. In: Parry, M.L., Canziani, O.F., Palutikof, J.P., van der Linden, P.J., Hanson, C.E. (Eds.), Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York. IPCC, “Summary for policymakers,” in Climate Change, 2014. Impacts, adaptation, and vulnerability. Part A: Global and sectoral aspects. In: Field, C.B., Barros, V.R., Dokken, D.J., et al.,Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, 2014. Cambridge University Press, Cambridge, UK, pp. 1
32. Available from: http://www.ipcc.ch/pdf/assessment-report/ ar5/wg2/ar5_wgII_spm.en.pdf. Jones, P.D., Lister, D.H., Jaggard, K.W., Pidgeon, J.D., 2003. Future climate impact on the productivity of sugar beet (Beta vulgaris l.) in Europe. Clim. Change 58, 93
108. Jones, B., O’Neill, B.C., McDaniel, L., McGinnis, S., Mearns, L.O., Claudia Tebaldi, C., 2015. Future population exposure to US heat extremes. Nat. Clim. Change 5, 652
655. Jongman, B., Winsemius, H.C., Aerts, J.C., de Perez, E.C., van Aalst, M.K., Kron, W., et al., 2015. Declining vulnerability to river floods and the global benefits of adaptation. Proc. Natl. Acad. Sci. U.S.A. 112, E2271
E2280. Available from: https://doi.org/10.1073/pnas.1414439112. Kaffka, S., Hembree, K., 2004. The effects of saline soil, irrigation, and seed treatments on sugar beet stand establishment. J. Sugar Beet Res. 41, 61
72. Kasim, W.A., Osman, M.E., Omar, M.N., Abd-El-Daim, I.A., Bejai, S., Meijer, J., 2013. Control of drought stress in wheat using plant-growth-promoting bacteria. J. Plant Growth Regul. 32, 122
130. Available from: https:// doi.org/10.1007/s00344-012-9283-7. Kates, R.W., Colten, C.E., Laska, S., Leatherman, S.P., 2006. Reconstruction of New Orleans after Hurricane Katrina: a research perspective. Proc. Natl. Acad. Sci. U.S.A. 103, 14653
14660. Available from: https://doi. org/10.1073/pnas.0605726103. PMID: 17003119. Kjellstrom, T., Kovats, R.S., Lloyd, S.J., Holt, T., Tol, R.S., 2009. The direct impact of climate change on regional labor productivity. Arch. Environ. Occup. Health 64, 217
227. Knox, J., Daccache, A., Hess, T., David Haro, D., 2016. Meta-analysis of climate impacts and uncertainty on crop yields in Europe. Environ. Res. Lett. 11, 113004. Kodra, E., Ganguly, A.R., 2014. Asymmetry of projected increases in extreme temperature distributions. Sci. Rep. 4, 5884. Koyro, H.-W., 2000. Effect of high NaCl-salinity on plant growth, leaf morphology, and ion composition in leaf tissues of Beta vulgaris ssp. Maritima. J. Appl. Bot. 74, 67
73. Kreibich, H., Thieken, A.H., 2009. Coping with floods in the city of Dresden, Germany. Nat. Hazards 51, 423
436. Available from: https://doi.org/10.1007/s11069-007-9200-8. Kurz, W.A., Dymond, C.C., Stinson, G., Rampley, G.J., Neilson, E.T., Carroll, A.L., et al., 2008. Mountain pine beetle and forest carbon feedback to climate change. Nature 452, 987
990. Available from: https://doi.org/ 10.1038/nature06777. Lal, R., 2004. Soils and sustainable agriculture: a review. Sustainable Agriculture. Springer, Netherlands, pp. 15
23. Available from: https://doi.org/10.1007/978-90-481-2666-8_3. Lesk, C., Coffel, E., D’Amato, A.W., Dodds, K., Horton, R., 2017. Threats to North American forests from southern pine beetle with warming winters. Nat. Clim. Change 7, 713
717. Liu, Y., Yang, Y., 2012. Spatial distribution of major natural disasters of China in historical period. Acta Geogr. Sin. 67, 291
300 (in Chinese). Lobell, D.B., Ba¨nziger, M., Magorokosho, C., Vivek, B., 2011. Nonlinear heat effects on African maize as evidenced by historical yield trials. Nat. Clim. Change 1, 42
45. Lobell, D.B., Baldos, U.L.C., Hertel, T.W., 2013. Climate adaptation as mitigation: the case of agricultural investments. Environ. Res. Lett. 8, 015012. Mahajan, S., Tuteja, N., 2005. Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139
158. Available from: https://doi.org/http://10.1016/j.abb.2005.10.018.

Plant Life under Changing Environment

References

909

MALR, 2017. Egyptian Ministry of Agricultural and Land Reclamation, Selected Data on Costs, Prices, and Land in Production, Statistical Year Book for Agriculture, 2017. MALR’s Sugar Croup Council. 2016. MALR, Ministry of Agriculture and Land Reclamation, Council of Sugary Crops Annual Report, Egypt, Various Issues. Statistical Year Book for the Ministry of Agriculture. Maplecroft, 2012. ,https://maplecroft.com/portfolio/new-analysis/2012/10/31/egypts-political-risk-landscapehinging-new-constitution-maplecroft-country-risk-briefing/.. Maqsood, L., Khalil, T.M., 2013. A review of direct and indirect implications of laser land leveling as agriculture resource conservation technology in Punjab Province of Pakistan. In: IEEE 2013 Global Humanitarian Technology Conference, pp. 349
354. Meehl, G.A., Tebaldi, C., 2004. More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994
997. Meehl, G.A., Collins, W.D., Boville, B.A., Kiehl, J.T., Wigley, T.M.L., Arblaster, J.M., 2000. Response of the NCAR climate system model to increased CO2 and the role of physical processes. J. Clim. 13, 1879
1898. Mehrandish, M., Moeini, M.M., Armin, M., 2013. Sugar beet (Beta vulgaris L.) response to potassium application under full and deficit irrigation. Eur. J. Exp. Biol. 2, 2113
2219. Mekki, B.B., 2014. Root yield and quality of sugar beet (Beta vulgaris L.) in response to foliar application with urea, zinc and manganese in newly reclaimed sandy soil. Am.-Eurasian J. Agric. Environ. Sci. 14, 800
806. Min, S.K., Zhang, X., Zwiers, F.W., Hegerl, G.C., 2011. Human contribution to more-intense precipitation extremes. Nature 470, 378
381. Minhas, P.S., Rane, J., Ratna Kumar Pasala, R.K., 2017. Abiotic stresses in agriculture: an overview. In: Minhas, P. S., et al., (Eds.), Abiotic Stress Management for Resilient Agriculture, 2017. Springer Nature Singapore Pvt Ltd, pp. 3
8. Miralles, D.G., Teuling, A.J., van Heerwaarden, C.C., Vila`-Guerau de Arellano, J., 2014. Mega-heatwave temperatures due to combined soil desiccation and atmospheric heat accumulation. Nat. Geosci. 7, 345
349. Mobtaker, H.G., Keyhani, A., Mohammadi, A., Rafiee, S., Akram, A., 2010. Sensitivity analysis of energy inputs for barley production in Hamedan Province of Iran. Agric. Ecosyst. Environ. 137, 367
372. Mohammadi, A., Omid, M., 2010. Econometrical analysis and relation between energy inputs and yield of greenhouse cucumber production in Iran. Appl. Energy 87, 191
196. Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651
681. Available from: https://doi.org/10.1146/annurev.arplant.59.032607.092911. MWRI, 2017. Egyptian Ministry of Water Resources and Irrigation, Selected Water Resources Data 2017. Neseim, M.R., Amin, A.Y., El-Mohammady, M.M.S., 2014. Effect of potassium applied with foliar spray of yeast on sugar beet growth and yield under drought stress. Global Adv. Res. J. Agric. Sci. 3, 211
222. Nicholls, R.J., Hoozemans, F.M.J., Marchand, M., 1999. Increasing flood risk and wetland losses due to global sealevel rise: regional and global analyses. Global Environ. Change 9, S69
S87. Available from: https://doi.org/ 10.1016/S0959-3780(99)00019-9. Oestigaard, T., 2012. When everything depends on the rain. Drought, rain-fed agriculture and food security. The Nordic Africa Institute Annual Report 2011: Africa’s Changing Societies: Reform from Below. The Nordic Africa Institute, Uppsala, pp. 24
25. Olesen, J.E., Bindi, M., 2002. Consequences of climate change for European agricultural productivity, land use and policy. Eur. J. Agron. 16, 239
262. Olesen, J.E., Carter, T.R., Diaz-Ambrona, C.H., Fronzek, S., Heidmann, T., Hickler, T., et al., 2007. Uncertainties in projected impacts of climate change on European agriculture and ecosystems based on scenarios from regional climate models. Clim. Change 81, 123
143. Ouda, S.M.M., 2001. Response of sugar beet to N and K fertilizers levels under sandy soil conditions. Zagazig J. Agric. Res. 28, 275
297. Owen, R., 1984. The study of Middle Eastern industrial history: notes on the interrelationship between factories and small-scale manufacturing with special references to Lebanese silk and Egyptian sugar, 1900
1930. Int. J. Middle East Stud. 16, 475
487. Ozkan, B., Kurklu, A., Akcaoz, H., 2004. An input-output energy analysis in greenhouse vegetable production: a case study for Antalya region of Turkey. Biomass Bioenergy 26, 89
95. Passioura, J.B., 2012. Phenotyping for drought tolerance in grain crops: when is it useful to breeders? Funct. Plant Biol. 39, 851. Available from: https://doi.org/10.1071/FP12079. Petkova, E.P., Horton, R.M., Bader, D.A., Kinney, P.L., 2013. Projected heat-related mortality in the U.S. urban northeast. Int. J. Environ. Res. Public Health 10, 6734
6747.

Plant Life under Changing Environment

910

37. Management of abiotic stress and sustainability

Pimentel, D., Berger, B., Filiberto, D., Newton, M., Wolfe, B., Karabinakis, E., et al., 2004. Water resources: agricultural and environmental issues. BioScience 54, 909
918. Porter, J.R., Xie, L., Challinor, A.J., Cochrane, K., Howden, M., Iqbal, M.M., et al., 2014. Chapter 7. Food security and food production systems. In: Climate Change 2014: Impacts, Adaptation and Vulnerability. Working Group II Contribution to the IPCC 5th Assessment Report, Geneva, Switzerland. Rafiee, S., Avval, S.H.M., Mohammadi, A., 2010. Modeling and sensitivity analysis of energy inputs for apple production in Iran. Energy 35, 3301
3306. Rahmstorf, S., Coumou, D., 2012. Increase of extreme events in a warming world. Proc. Natl. Acad. Sci. U.S.A. 109, 4708
4788. Rao, S., Klimont, Z., Leitao, J., Riahi, K., van Dingenen, R., Reis, L.A., et al., 2016. A multi-model assessment of the co-benefits of climate mitigation for global air quality. Environ. Res. Lett. 11, 124013. Rebetzke, G.J., van Herwaarden, A., Biddulph, B., Chenu, K., Moeller, C., Richards, R.A., et al., 2012. Protocols for Experimental Plot Sampling, Handling and Processing of Cereal Experiments
Standardised Methods for Use in Field Studies. Prometheus Wiki. CSIRO Publishing, Collingwood. Available at ,http://prometheuswiki.publish.csiro.au/tiki-index.php. [verified October 2012]. Reda, K.A., Shalaby, A.A., Kishk, H.T., Hegazi, A.M., 1980. Some effects of potassium on growth yield and chemical composition of beet irrigated with saline water containing different levels of boron. Ain Shams Univ., Fac. Agric., Res. Bull. 12337, 16 pp. Regato, P., Korakaki, E., 2010. The Mediterranean Forests Against Global Climate Change. Publications: WWF Greece, p. 106. Rengasamy, P., 2006. World salinization with emphasis on Australia. J. Exp. Bot. 57, 1017
1023. Available from: https://doi.org/10.1093/jxb/erj108. Rodrı´guez-Dı´az, J.A., Camacho-Poyato, E., Blanco-Pe´rez, M., 2011. Evaluation of water and energy use in pressurized irrigation networks in Southern Spain. J. Irrig. Drain. Eng. Available from: https://doi.org/10.1061/ (ASCE)IR.1943-4774.0000338. Rosenzweig, C., Iglesias, A., Yang, X.B., Eric, C., 2001. Climate change and extreme weather events; implications for food production, plant diseases, and pests. Global Change Hum. Health 2, 90
104. Rosenzweig, C., Elliott, J., Deryng, D., Ruane, A.C., Mu¨ller, C., Arneth, A., et al., 2014. Assessing agricultural risks of climate change in the 21st century in a global gridded crop model intercomparison. Proc. Natl. Acad. Sci. U. S.A. 111, 3268
3273. Available from: https://doi.org/10.1073/pnas.1222463110. Epub 2013 Dec 16. Sadeghian, S.Y., Yavari, N., 2004. Effect of water-deficit stress on germination and early seedling growth in sugar beet. J. Agron. Crop Sci. 190, 138
144. Samavatean, N., Rafiee, S., Mobli, H., Mohammadi, A., 2011. An analysis of energy use and relation between energy inputs and yield, costs and income of garlic production in Iran. Renew. Energy 36, 1808
1813. Saxena, N.P., 1985. The role of potassium in drought tolerance. Potash Rev. 16, 102. Shahbaz, M., Ashraf, M., 2013. Improving salinity tolerance in cereals. Crit. Rev. Plant Sci. 32, 237
249. Sharma, U., Paliyal, S.S., Sharma, S.P., Sharma, G.D., 2014. Effects of continuous use of chemical fertilizers and manure on soil fertility and productivity of maize
wheat under rainfed conditions of the Western Himalayas. Commun. Soil Sci. Plant Anal. 45, 2647
2659. Available from: https://doi.org/10.1080/00103624.2014.941854. Shehata, M.M., Shohair, A.A., Mostafa, S.N., 2000. The effect of soil moisture level on four sugar beet varieties. Egypt. J. Agric. Res. 78, 1141
1160. Shi, P.J., 2005. Theory and practice on disaster system research in a fourth time. J. Nat. Disasters 14, 1
7 (in Chinese). Shrivastava, P., Kumar, R., 2015. ): Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 22, 123
131. Smith, P., Gregory, P.J., 2013. Climate change and sustainable food production. Proc. Nutr. Soc. 72, 21
28. Smith, P., Haberl, H., Popp, A., Erb, K.-H., Lauk, C., Harper, R., et al., 2013. How much land-based greenhouse gas mitigation can be achieved without compromising food security and environmental goals? Global Change Biol. 19, 2285
2302. Stott, P.A., Stone, D.A., Allen, M.R., 2004. Human contribution to the European heatwave of 2003. Nature 432, 610
614. Sulmon, C., VanBaaren, J., Cabello-Hurtado, F., Gouesbet, G., Hennion, F., Mony, C., et al., 2015. Abiotic stressors and stress responses: what commonalities appear between species across biological organization levels? Environ. Pollut. 202, 66
77. Available from: https://doi.org/10.1016/j.envpol.2015.03.013.

Plant Life under Changing Environment

References

911

TemIzel, K.E., AkIn, F., Aydogan, D., Eren, S., Kevseroglu, K., 2012. Determination the effect of land leveling on soil loses in rice (Oryza sativa L.) production areas. Bulg. J. Agric. Sci. 18, 219
226. Tiwari, K.N., Sharma, S.K., Singh, V.K., Dwivedi, B.S., Shukla, A.K., 2006. Site-specific nutrient management for increasing crop productivity in India. Results with Rice-Wheat and Rice-Rice Systems. PDCSR, Modipuram and PPIC-India Programme, Gurgaon, p. 112. Tsialtas, J.T., Maslaris, N., 2005. Effect of N fertilization rate on sugar yield and non-sugar impurities of sugar beets (Beta vulgaris) grown under Mediterranean conditions. J. Agron. Crop Sci. 191, 330
339. Tsialtas, J.T., Maslaris, N., 2006. Leaf carbon isotope discrimination relationships to element content in soil, roots and leaves of sugar beets grown under Mediterranean conditions. Field Crops Res. 99, 125
135. Tzilivakis, J., Warner, D.J., May, M., Lewis, K.A., Jaggard, K., 2005. An assessment of the energy inputs and greenhouse gas emissions in sugar beet (Beta vulgaris) production in the UK. Agric. Syst. 85, 101
119. United States Department of Agriculture, 2012. Foreign Agricultural Service (USDA FAS 2012). ,https://www. fas.usda.gov/search/2012.. Urban, D., Roberts, M.J., Schlenker, W., Lobell, D.B., 2012. Projected temperature changes indicate significant increase in inter-annual variability of U.S. maize yields. Clim. Change 112, 525
533. Venkateswarlu, B., Shanker, A.K., 2009. Climate change and agriculture: adaptation and mitigation strategies. Indian J. Agron. 54, 226
230. Vermeulen, S.J., Campbell, B.M., Ingram, J.S.I., 2012. Climate change and food systems. Annu. Rev. Environ. Resour. 37, 195
222. Vinocur, B., Altman, A., 2005. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr. Opin. Biotechnol. 16, 123
132. Vurukonda, S.S., Vardharajula, S., Shrivastava, M., SkZ, A., 2016. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol. Res. 184, 13
24. Available from: https://doi.org/ 10.1016/j.micres.2015.12.003. Wakeel, A., Abd-El-Motagally, F., Steffens, D., Schubert, S., 2009. Sodium-induced calcium deficiency in sugar beet during substitution of potassium by sodium. J. Plant Nutr. Soil Sci. 172, 254
260. Wallace, J.S., Acreman, M.C., Sullivan, C.A., 2003. The sharing ofwaterbetweensocietyandecosystems:fromconflicttocatchment
basedco
management. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 358, 2011
2026. Wang, W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1
14. Available from: https://doi.org/http://10.1007/ s00425-003-1105-5. Wang, S.M., Wan, C.G., Wang, Y.R., Chen, H., Zhou, Z.Y., Fu, H., et al., 2004. The characteristics of Na1, K1 and free proline distribution in several drought-resistant plants of the Alxa Desert, China. J. Arid Environ. 56, 525
539. Wang, M., Zheng, Q., Shen, Q., Guo, S., 2013. The critical role of potassium in plant stress response. Int. J. Mol. Sci. 14, 7370
7390. Available from: https://doi.org/10.3390/ijms14047370. Wheeler, T., VonBraun, J., 2013. Climate change impacts on global food security. Science 341, 508
513. Available from: https://doi.org/10.1126/science.1239402. Wind, H.G., Nierop, T.M., De Blois, C.J., De Kok, J.L., 1999. Analysis of flood damages from the 1993 and 1995 Meuse floods. Water Resour. Res. 35, 3459
3465. Available from: https://doi.org/10.1029/1999WR900192. Woodward, M., Gouldby, B., Kapelan, Z., Khu, S.-T., Townend, I., 2011. Real options in flood risk management decision making. J. Flood Risk Manage. 4, 339
349. Available from: https://doi.org/10.1111/j.1753318X.2011.01119.x. WorldAtlas, 2018. World sugar beet production countries in the world by 1000 tonnes 2018. Available from: ,https://knoema.com/atlas/topics/Agriculture/Crops-Production-Quantity-tonnes/Sugar-beet-production.. World Bank, 2012. Beyond Scarcity: Water Security in the Middle East and North Africa. Xin, Z., Browse, J., 2001. Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ. 23, 893
902. Yordanov, I., Velikova, V., Tsonev, T., 2000. Plant responses to drought, acclimation, and stress tolerance. Photosynthetica 38, 171
186. Zommers, Z., van der Geest, K., De Sherbinin, A., Kienberger, S., Roberts, E., Harootunian, G., et al., 2016. Loss and Damage: The Role of Ecosystem Services. United National Environment Programme, Nairobi, p. 84. Zurich, 2014. Risk Nexus, Central European Floods 2013: A Retrospective, Zurich, Zurich, Switzerland.

Plant Life under Changing Environment

912

37. Management of abiotic stress and sustainability

Further reading FAO, 2012. Food and Agriculture Organization. World Water Day 2012 Celebration. Un Conference Centre, Bangkok, 22 March 2012. Available online ,http://www.Fao.Org/asiapacific/rap/home/meetings/list/ detail/en/?Meetings_id 5 637&year 5 2012. (accessed 20.08.16.). Sources. ,http://en.wikipedia.org/wiki/2013_North_India_Floods.; ,http://en.wikipedia.org/wiki/2010_ Pakistan_Floods.; ,http//en.wikipedia.org/wiki/Floods_in_the_United_states:_2001%E2%80%93present..

Appendix

Future of sugar beet industry (FOSI)

Future of sugar beet industry (FOSI) in old land of governorate Kafr-El Sheikh Future of sugar beet industry (FOSI) in old land of Egypt Future of sugar beet industry (FOSI) in old land of governorate Gharbia

Future of sugar beet industry (FOSI) in new land of Egypt

Future of sugar beet industry (FOSI) in new land of governorate Kafr El-Sheikh

Future of sugar beet industry (FOSI) in new land of governorate Gharbia

FIGURE 37.10 Structure model of FOSI and water scarcity in North Egypt. FOSI, Future of sugar industry. Source: FOSI (2017).

The structure of the FOSI model is presented in Fig. 37.10 and can be written as follows: “Maximize

F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

[(AFuture-of-sugar-industry-in-North-Egypt 2BFuture-of-sugar-industry-in-North-Egypt)3CFuture-of-sugarindustry-in-North-Egypt]1[(DFuture-of-sugar-industry-in-North-Egypt 3CFuture-of-sugar-industry-in-NorthEgypt)/(EFuture-of-sugar-industry-in-North-Egypt)3100]1[(DFuture-of-sugar-industry-in-NorthEgypt 3CFuture-of-sugar-industry-in-North-Egypt)/(FFuture-of-sugar-industry-in-North-Egypt)3100]1 [(DFuture-of-sugar-industry-in-North-Egypt 3CFuture-of-sugar-industry-in-North-Egypt)/(GFuture-of-sugarindustry-in-North-Egypt)3100]1[(DFuture-of-sugar-industry-in-North-Egypt 3CFuture-of-sugar-industry-inNorth-Egypt)/(HFuture-of-sugar-industry-in-North-Egypt)3100] (1)”

Plant Life under Changing Environment

Appendix

Subject

to“

913

F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

AFuture-of-sugar-industry-in-North-Egypt $MAX_Af for Af (2) F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

sugar-industry-in-North-Egypt #MIN_Bf

BFuture-of-

for Bf (3)

F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

sugar-industry-in-North-Egypt $MAX_Cf

for Cf (4)

F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

sugar-industry-in-North-Egypt $MAX_Df

CFuture-of-

DFuture-of-

for Df (5)

F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

EFuture-of-sugar-industry-in-North-Egypt $ MAX_Ef for Ef (6) F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

sugar-industry-in-North-Egypt $MAX_Ff

for Ff (7)

F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

sugar-industry-in-North-Egypt $MAX_Gf

GFuture-of-

for Gf (8)

F P U P T P U P R P E P O P F P S P U P G P A P R P I P N P D P U P S P T P R P Y P I P N P N P O P R P T P H P E P G P Y P P P T P f51 u51 t51 u51 r51 e51 o51 f51 s51 u51 g51 a51 r51 i51 n51 d51 u51 s51 t51 r51 y51 i51 n51 n51 o51 r51 t51 h51 e51 g51 y51 p51 t51

sugar-industry-in-North-Egypt $MAX_Hf

FFuture-of-

HFuture-of-

for Hf (9)”

“MAX_Af Maximum revenue for planting sugar crop variety f (10)” “MIN_Bf Minimum total costs for planting sugar crop variety f (11)” “MAX_Cf Maximum land area available for planting sugar crop variety f (12)” “MAX_Df Maximum sugar crop yield in planting sugar crop variety f (13)” “MAX_Ef Maximum working sugar beet factory efficiency for sugar crop variety f (14)” “MAX_Ff Maximum secondary crop of sugar crop variety f for feeding animals (15)” “MAX_Gf Maximum production of sugar crop variety f in the case of climate change (16)” “MAX_Hf Maximum sugar beet variety seeds for planting in sugar beet farms f (17)” “MIN_If Maximum main sugar crop price in planting sugar crop variety f (18)” “MIN_Jf Maximum secondary sugar crop price in planting sugar crop variety f (16)” “MIN_Kf Maximum labor wages cost in planting sugar crop variety f (17)” “MIN_Lf Minimum draft animals cost in planting sugar crop variety f (18)” “MIN_Mf Minimum machinery cost in planting sugar crop variety f (19)” “MIN_Nf Minimum seed cost in planting sugar crop variety f (20)” “MIN_Of Minimum manure cost in planting sugar crop variety f (21)” “MIN_Pf Minimum fertilizer cost in planting sugar crop variety f (22)”

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37. Management of abiotic stress and sustainability

“MIN_Qf Minimum insecticide cost in planting sugar crop variety f (23)” “MIN_Rf Minimum laser land leveling cost in planting sugar crop variety f (24)” “MAX_Sf Maximum other expenses’ cost in planting sugar crop variety f (25)” “MIN_Tf Minimum rent cost in planting sugar crop variety f (26)” “MIN_Uf Minimum sugar crop water consumption in planting sugar crop variety f (27)” “MIN_Nf Minimum fertilizer use in cultivation in planting sugar crop variety f (28)” “MIN_Vf Minimum energy use in cultivation in planting sugar crop variety f (29)” “MIN_Vf Minimum CO2 emission in cultivation in planting sugar crop variety f (30)” Variables “AFuture-of-sugar-industry-in-North-Egypt Estimated revenue for planting main crop yield f and secondary crop yield u of sugar crop variety t of sugar crop u in subsugar crop-group r in subsoil type e (Old land or New land) in subzone (North Egypt) o in subseason f by total crop production cost s include labor wages cost u draft animals cost g machinery cost a seeds cost r manure coast i fertilizers coast n insecticides coast d laser land leveling cost u rent cost s and other expenses coast t by total energy consumptions r include energy consumption for irrigation y energy consumption for labor i energy consumption for draft animal n energy consumption for land preparation n energy consumption for seed planting o energy consumption for manure r energy consumption for fertilization t energy consumption for insecticide h energy consumption for laser land leveling e and energy consumption for other expenses g by total kerosene fuel consumption y crop water consumption p and crop emission t.” “BFuture-of-sugar-industry-in-North-Egypt Estimated total costs of planting main crop yield f and secondary crop yield u of sugar crop variety t of sugar crop u in subsugar crop-group r in subsoil type e (Old land or New land) in subzone (North Egypt) o in subseason f by total crop production cost s include labor wages cost u draft animals cost g machinery cost a seeds cost r manure coast i fertilizers coast n insecticides coast d laser land leveling cost u rent cost s and other expenses coast t by total energy consumptions r include energy consumption for irrigation y energy consumption for labor i energy consumption for draft animal n energy consumption for land preparation n energy consumption for seed planting o energy consumption for manure r energy consumption for fertilization t energy consumption for insecticide h energy consumption for laser land leveling e and energy consumption for other expenses g by total kerosene fuel consumption y crop water consumption p and crop emission t.” “CFuture-of-sugar-industry-in-North-Egypt Estimated land area allocated for planting main crop yield f and secondary crop yield u of sugar crop variety t of sugar crop u in subsugar crop-group r in subsoil type e (Old land or New land) in subzone (North Egypt) o in subseason f by total crop production cost s include labor wages cost u draft animals cost g machinery cost a seeds cost r manure coast i fertilizers coast n insecticides coast d laser land leveling cost u rent cost s and other expenses coast t by total energy consumptions r include energy consumption for irrigation y energy consumption for labor i energy consumption for draft animal n energy consumption for land preparation n energy consumption for seed planting o energy consumption for manure r energy consumption for fertilization t energy consumption for insecticide h energy consumption for laser land leveling e and energy consumption for other expenses g by total kerosene fuel consumption y crop water consumption p and crop emission t.”

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Appendix

915

“DFuture-of-sugar-industry-in-North-Egypt Estimated sugar crop variety yield production allocated in planting main crop yield f and secondary crop yield u of sugar crop variety t of sugar crop u in subsugar crop-group r in subsoil type e (Old land or New land) in subzone (North Egypt) o in subseason f by total crop production cost s include labor wages cost u draft animals cost g machinery cost a seeds cost r manure coast i fertilizers coast n insecticides coast d laser land leveling cost u rent cost s and other expenses coast t by total energy consumptions r include energy consumption for irrigation y energy consumption for labor i energy consumption for draft animal n energy consumption for land preparation n energy consumption for seed planting o energy consumption for manure r energy consumption for fertilization t energy consumption for insecticide h energy consumption for laser land leveling e and energy consumption for other expenses g by total kerosene fuel consumption y crop water consumption p and crop emission t.” “EFuture-of-sugar-industry-in-North-Egypt Estimated sugar beet variety production, for working the sugar beet factory in this governorate in high efficiency and give high production of sugar, from main crop yield f and secondary crop yield u of sugar crop variety t of sugar crop u in subsugar crop-group r in subsoil type e (Old land or New land) in subzone (North Egypt) o in subseason f by total crop production cost s include labor wages cost u draft animals cost g machinery cost a seeds cost r manure coast i fertilizers coast n insecticides coast d laser land leveling cost u rent cost s and other expenses coast t by total energy consumptions r include energy consumption for irrigation y energy consumption for labor i energy consumption for draft animal n energy consumption for land preparation n energy consumption for seed planting o energy consumption for manure r energy consumption for fertilization t energy consumption for insecticide h energy consumption for laser land leveling e and energy consumption for other expenses g by total kerosene fuel consumption y crop water consumption p and crop emission t.” “FFuture-of-sugar-industry-in-North-Egypt Estimated secondary production of sugar beet variety, for working the animals farms in this governorate in high efficiency and give high production, from main crop yield f and secondary crop yield u of sugar crop variety t of sugar crop u in subsugar crop-group r in subsoil type e (Old land or New land) in subzone (North Egypt) o in subseason f by total crop production cost s include labor wages cost u draft animals cost g machinery cost a seeds cost r manure coast i fertilizers coast n insecticides coast d laser land leveling cost u rent cost s and other expenses coast t by total energy consumptions r include energy consumption for irrigation y energy consumption for labor i energy consumption for draft animal n energy consumption for land preparation n energy consumption for seed planting o energy consumption for manure r energy consumption for fertilization t energy consumption for insecticide h energy consumption for laser land leveling e and energy consumption for other expenses g by total kerosene fuel consumption y crop water consumption p and crop emission t.” “GFuture-of-sugar-industry-in-North-Egypt Estimated sugar beet variety production, in the case of climate change, salinity in case the of rising Mediterranean sea level in every governorate in north Egypt, in high quality, from main crop yield f and secondary crop yield u of sugar crop variety t of sugar crop u in subsugar crop-group r in subsoil type e (Old land or New land) in subzone (North Egypt) o in subseason f by total crop production cost s include labor wages cost u draft animals cost g machinery cost a seeds cost r manure coast i fertilizers coast n insecticides coast d laser land leveling cost u rent cost s and other

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37. Management of abiotic stress and sustainability

expenses coast t by total energy consumptions r include energy consumption for irrigation y energy consumption for labor i energy consumption for draft animal n energy consumption for land preparation n energy consumption for seed planting o energy consumption for manure r energy consumption for fertilization t energy consumption for insecticide h energy consumption for laser land leveling e and energy consumption for other expenses g by total kerosene fuel consumption y crop water consumption p and crop emission t.” “HFuture-of-sugar-industry-in-North-Egypt Estimated sugar beet variety seeds for planting sugarcane farms in every governorate, from main crop yield f and secondary crop yield u of sugar crop variety t of sugar crop u in subsugar crop-group r in subsoil type e (Old land or New land) in subzone (North Egypt) o in subseason f by total crop production cost s include labor wages cost u draft animals cost g machinery cost a seeds cost r manure coast i fertilizers coast n insecticides coast d laser land leveling cost u rent cost s and other expenses coast t by total energy consumptions r include energy consumption for irrigation y energy consumption for labor i energy consumption for draft animal n energy consumption for land preparation n energy consumption for seed planting o energy consumption for manure r energy consumption for fertilization t energy consumption for insecticide h energy consumption for laser land leveling e and energy consumption for other expenses g by total kerosene fuel consumption y crop water consumption p and crop emission t.”

Plant Life under Changing Environment

C H A P T E R

38 Use of quantitative trait loci to develop stress tolerance in plants Dev Paudel1, Smit Dhakal2, Saroj Parajuli1, Laxman Adhikari3, Ze Peng1, You Qian1, Dipendra Shahi1, Muhsin Avci1, Shiva O. Makaju4 and Baskaran Kannan1 1

University of Florida, Gainesville, FL, United States 2University of Illinois-Urbana Champaign, Urbana, IL, United States 3Kansas State University, Manhattan, KS, United States 4 University of Georgia, Athens, GA, United States

38.1 Introduction Quantitative trait loci (QTLs) refer to specific regions on chromosome that harbor gene (s) controlling traits (Miles and Wayne, 2008). QTL mapping tries to identify these stretches of DNA that are closely linked to genes underlying a specific trait by performing statistical analysis of molecular markers and traits in populations of controlled crosses (Stinchcombe and Hoekstra, 2008). QTL mapping provides a starting point for dissecting complex traits into its component alleles. It helps to quantify the relative effects of alleles on the traits and locate genomic regions responsible for marker trait association. It also provides a foundation of marker-assisted selection (MAS) that expedites the breeding process given the proper estimation of position and effects of QTLs (Doerge, 2002). QTLs that are detected in multiple environments are called stable QTL (sQTL) and are reliable for MAS. Mapping loci on genome requires a population that segregates for the target traits. QTL analysis is performed by estimating correlation between phenotype data with genotype (markers) data of segregating populations (Miles and Wayne, 2008). Primary types of segregating populations for QTL mapping include F2, recombinant inbred lines (RILs), backcross 1 (BC1), double haploid lines (DHLs), near-isogenic lines (NILs), and full-sib F1 (pseudo-testcross) (Schneider, 2005). When multiple traits QTLs are detected in the same region or within the confidence interval (CI) region of each QTL, that is, overlapping CI, they are termed QTL cluster or

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coincident QTL (cQTL) (Zhou et al., 2018). These cQTLs are potentially important QTLs that control the traits. Major QTLs typically account for a large amount ( . 10%) of the total explained phenotypic variation while minor QTLs generally account for ,10% of the total explained phenotypic variation. Many mapping methodologies can be employed to detect QTLs, namely, linkage, association, NIL, F2 or BC. Classical biparental linkage mapping involves a two-parent cross for the contrasting trait(s) (Portis et al., 2015). It utilizes linkage between two loci and recombination, whereas in association mapping (AM), variation present in natural population without definite family structure is utilized. It utilizes linkage disequilibrium between loci to detect the marker trait association. For detection in AM a locus must have an effect in multiple lines. However, in biparental cross population, a single locus might show a major effect (Wang et al., 2008). QTL metaanalysis evaluates information about a QTL for same/similar traits from multiple environments in separate experiments. It determines whether these QTLs from different experiments represent a single locus and reduce the CI of the QTLs by refining their position (Arcade et al., 2004). QTLs identified in conventional QTL analysis are often confounded by background noise due to the influence of trait expression itself and genetic interrelationship between two testing conditions. Unconditional/conventional QTL analysis uses phenotypic values of traits itself. Value predicted from unconditional QTL analysis refers to the accumulative gene effects due to normal as well as stressed condition. Because of this, additional QTL with small effects go undetected in unconditional QTL analysis. Conditional QTL analysis uses conditional phenotypic values of traits, that is, values detected under stressed condition given those found under normal condition. In such analysis, normal-condition phenotypic value serves as an estimation of the genetic effect of the trait under stressed condition to calculate the effect value caused by specific stress (Zhang et al., 2010; Zhang and Wang, 2015). The advancement of next-generation sequencing has hugely facilitated QTL identification and mapping. High-density genetic maps developed by genotyping-by-sequencing (GBS) have been recently used to successfully identify many QTLs in various species. QTLs controlling plant abiotic stress such as extreme environmental responses—cold, heat, salinity, frost, and drought—have been detected for limited plant species. Nevertheless, the genetic mechanisms of stress tolerance are very complex and not fully understood for several plant species. This article reviews current literature on the identification and manipulation of genomic locations governing abiotic stress tolerance in plants.

38.2 Types of abiotic stress in plants The following abiotic stresses commonly affect plant performance (Fig. 38.1).

38.2.1 Drought stress Drought is a serious issue faced by modern global agriculture that causes tremendous yield losses. The 2012 drought in the United States caused loss of USD 21.6 billion in maize (Elliott et al., 2018), while the economic losses in agriculture caused by severe

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FIGURE 38.1 Abiotic stresses affecting plant performance.

drought were estimated to be approximately USD 6 billion between 2001 and 2016 in Brazil (Gutie´rrez et al., 2014). Yield losses caused by drought can be up to 50% 90% in rice (Oryza sativa L.) (Zhang et al., 2018a). Arid and dry lands have continued to increase considerably since the middle of the 20th century, and short- and long-term droughts are predicted to be, respectively, two and three times more common for most regions of the world (Basto et al, 2018). Thus improving drought tolerance in crops is a major objective in agriculture. Drought resistance has been mainly studied through mechanisms and QTLs involved in cellular or plant responses facilitating acclimation to drought conditions (Varshney et al., 2018a). Drought stress usually induces different responses from different tissues or organs. One of the most important aspects for improving the performance of plants under drought conditions is related to the roots, since health and vigor of the roots directly affect the plants’ capability to access water (Langridge and Reynolds, 2015). In addition, to study drought tolerance, a series of other traits associated with drought tolerance have also been studied, such as plant architecture, photosynthesis, resource allocation to roots or shoots, and osmotic traits. With efforts from research community, current research has been directed to a position where the manipulation of QTLs involved in drought tolerance becomes possible (Varshney et al., 2018a). In barley, several studies applied wild introgression lines (IL) representing exotic germplasms for QTL mapping. In one study a set of 47 wild barley IL was evaluated for drought stress responses, including growth and biomass parameters (Honsdorf et al., 2014a). Several favorable alleles for growth and biomass were identified. Particularly, one QTL led to an increase of biomass by 36%. In addition, 52 barley IL were used to identify QTLs involved in plant biomass and leaf senescence (Honsdorf et al., 2014b). Three QTLs leading to increased biomass and relative water content under drought were recommended for use in future-breeding programs to enhance drought tolerance. Kalladan et al. (2013)

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utilized a DH population obtained by crossing cultivated and wild accession parents to study seed quality and yield of barley in postanthesis drought conditions. They identified seven QTL regions. These studies represented efforts in using wild barley to increase the genetic variations for drought tolerance. Moreover, other parameters were also investigated such as chlorophyll fluorescence parameters indicating photosynthesis under postflowering drought (Guo et al., 2008). Those results could guide MAS applications aiming at introducing drought tolerance QTLs into ideal barley genotypes. In maize, root architecture related characteristics such as length, diameter, weight, and elongation of roots were studied in well-watered and water-stressed conditions (Tuberosa et al., 2002; Burton et al., 2014; Ruta et al., 2010; Landi et al., 2010). A population comprising 208 RILs was created by crossing drought-tolerant and drought-sensitive parents and used for discovering QTLs controlling root growth and responses to dehydration (Ruta et al., 2010). In this study, 13 QTLs were identified including two major QTLs for general vigor and constitutive increase in root elongation. Another study developed NILs for further characterization of a major QTL affecting root and agronomic traits in different water conditions (Landi et al., 2010). Results demonstrated that this QTL had a major constitutive effect on root characteristics, plant vigor, and productivity under different water conditions, genetic backgrounds, or inbreeding levels. Thus it is a promising candidate for cloning and application of MAS in maize. Some groups have also identified QTLs conveying drought tolerance via other characteristics such as leaf growth (Welcker et al., 2006), leaf temperature, shoot weight (Liu et al., 2011), leaf greenness, and plant senescence (Messmer et al., 2011). These researches provided valuable resources to improve drought tolerance in maize. In beans, Trapp et al. (2016) evaluated 19 stress response related traits in 20 plants each from extremely tolerant and susceptible lines of a RIL population. Among these 19 traits, 8 traits were associated with drought stress. This study provides an example of using extreme lines to validate previously identified QTLs and, specifically, confirmed the effect of two major QTLs related to responses to terminal drought. Another study focused on evaluating rooting pattern traits under drought stress and nonstress conditions in a RIL population, which identified 15 QTLs for both rooting pattern and shoot traits (Asfaw and Blair, 2012). This research also showed that the QTLs, related to root traits, were conditioned through constitutive gene expressions and that improving root traits, such as deep rooting, and increasing root length (RL) distribution are feasible for molecular breeding in common bean. Drought tolerance in pearl millet has been investigated through QTL mapping (Yadav et al., 2002). Many QTLs that were associated with drought tolerance specifically during reproductive stage were identified, among which one QTL explained 23% of the phenotypic variation. This study demonstrated the suitability of using marker-assisted BC (MABC) to introduce target QTLs to elite parent lines to improve productivity of pearl millet under drought conditions. In pearl millet, transpiration rate is an important parameter associated with drought tolerance. Under water-limited conditions a lower transpiration rate is desired, such that more water can be used for grain-filling period (Kholova´ et al., 2012). A RIL population was utilized for the evaluation of transpiration rate as well as other traits including leaf area, thickness, and organ weight (Kholova´ et al., 2012). Several alleles involved in controlling the transpiration rate comapped to a major QTL

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found earlier that was responsible for terminal drought tolerance. Another allele that enhanced dry biomass weight also comapped to a previous QTL associated with stover yield and tillering. This result showed that the alleles influencing water use of pearl millet could interact with each other as well as with the environment. Thus specific allele combinations could be desired for specific adaptation to different terminal drought conditions. The association between water saving and a lower transpiration rate was further demonstrated by identifying QTLs leading to decreased transpiration rate and those associated with grain weight and panicle harvest index (Aparna et al., 2015). These QTLs offered considerable potential for improving drought tolerance through MAS in pearl millet. Drought tolerance has also been studied using root, shoot, and other plant architecture traits in species such as cotton (Abdelraheem et al., 2015; Saranga et al., 2004), Brassica napus (Li et al., 2014a,b), chickpea (Varshney et al., 2014), and lentil (Idrissi et al., 2016). 38.2.1.1 Hormonal response under drought Continuous water deficit is known to cause hormonal changes in plants. Abscisic acid (ABA) concentration in leaves is affected by a reduced water availability. ABA is a stress hormone and is associated with drought tolerance where it mediates stomatal closure and promotes cuticular wax biosynthesis (Nambara and Kuchitsu, 2011). An increase in ABA concentration during water stress is a significant adaptive response of the plant to decreased available water (Aimar et al., 2011). Hence, ABA concentration can be used as a physiological trait to improve yield potential under drought stress. However, leaf ABA concentration of drought-stressed plants is quantitative in nature, making it difficult to select through traditional breeding program. QTL mapping is very useful alternative for selection of this polygenic trait. QTLs associated to leaf ABA have been identified in different crops such as maize (Zea mays) (Tuberosa et al., 1998), triticale (Triticosecale) (Zur et al., 2012), and wheat (Triticum aestivum) (Quarrie et al., 1994). The complex control of leaf ABA in maize was revealed by 16 and 17 QTLs reported, respectively, by Tuberosa et al. (1998) and Sanguineti et al. (1999). A single QTL controlling ABA in wheat was reported using DH population (Quarrie et al., 1994). In triticale, four QTLs regulating ABA accumulation under low temperature stress were identified (Zur et al., 2012). 38.2.1.2 Water-use and photosynthetic activity under drought Water use efficiency (WUE) provides plants with a much-needed advantage under drought stress. One way of assessing WUE is measuring stable carbon isotope ratio, Δ13C, of leaves, where variation in Δ13C reflects the differences in the partial pressure of CO2 inside the leaves. Since carbon isotope discrimination (CID) has a negative relationship with WUE, it can be used as an indirect method to select yield potential in drought (Juenger et al., 2005). Juenger et al. (2005) successfully mapped five QTLs affecting Δ13C in Arabidopsis. Likewise, a major QTL for CID was identified in barley utilizing RIL population (Chen et al., 2012). A study carried out by (Takai et al., 2009) also found a single QTL controlling Δ13C in rice. Three QTLs affecting CID in soybean have also been reported (Specht et al., 1986). Similarly, water stress causes decrease in photosynthetic gas exchange, modification in carbohydrate metabolism, and large change in hexose/sucrose metabolism. Four and nine

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QTLs were detected in maize for acid soluble invertase activity in control and stressed plants, respectively (Pelleschi et al., 1999). QTL mapping for photosynthetic traits such as gas exchange and chlorophyll fluorescence under drought and irrigated conditions has identified five, three, and four QTLs for net photosynthesis rate, stomatal conductance, and drought sensitivity, respectively (Gu et al., 2012). Two QTLs for net photosynthesis and one QTL for stomatal movement and water status were reported by Herve´ et al. (2001). 38.2.1.3 Osmotic adjustment under drought Osmotic adjustment (OA) in response to water deficits is an adaptive mechanism for drought tolerance in cereals through which plants maintain cell turgor when plants are exposed to water deficit and maintains vital processes of cells (Turner, 2018). In barley the OA capacity of a total of 187 RILs under different water treatments was evaluated (Teulat et al., 1998). Several conserved QTLs on chromosome 1 (7H) were identified for OA. In rice a major QTL associated with OA was identified, which was also close to genomic regions related to root morphology (Lilley et al., 1996). Another study in rice investigated both OA and root traits using a DH population, comprising 154 lines, and identified 41 QTLs explaining 8% 38% of the phenotypic variations (Zhang et al., 2001). A major QTL for OA and dehydration tolerance in rice using RILs of lowland cultivar CO9 3 Moroberekan and upland Japonica cultivar was identified (Lilley et al., 1996), whereas Zhang et al. (2001) reported five QTLs for OA in rice under drought using DHLs of CT9993 3 IR62266. In barley, Teulat et al. (1998) identified two genomic regions controlling OA traits. restriction fragment length polymorphism (RFLP) analysis in wheat suggested that the osmoregulation gene was located on chromosome 7A (Morgan and Tan, 1996). Similarly, Kiani et al. (2007) also reported a QTL controlling OA in sunflower. 38.2.1.4 Root responses under drought Under drought stress, plants maintain metabolic activities through drought avoidance or dehydration tolerance mechanisms. Drought avoidance is a physiological process in which plant cells maintain high water potential and increase WUE. This can be done using various processes such as reducing transpiration, extracting more water from the roots, increasing root growth, and limiting vegetative growth (Kooyers, 2015). Dehydration tolerance is a mechanism of maintaining high tolerance to desiccation by OA and cell membrane stability (CMS). CMS is the ability of cell membrane to restrict water stress damage and to regain integrity and membrane bound actions promptly upon rehydration. It can be measured by checking electrolyte leakage from a segment of leaf (Bajji et al., 2002). Deep root system attributes to the mechanism of drought avoidance in plants as they primarily absorb and translocate water and nutrients from soil besides supporting the plant’s stature. Deep and thicker root system also allows the plants to access water from deep soil horizon, which is usually inaccessible to shallow-rooted plants. As an important staple food crop, rice, which is grown on irrigated lands, is prone to being severely affected by drought. The study of deep rooting in rice is usually carried out using “basket” method by evaluating the ratio of deep rooting (RDR), which is an index of downward root growth (Uga et al., 2011). A major QTL involved in RDR was found on the chromosome 9 in rice (Uga et al., 2011). The QTL deeper rooting 1 (Dro1) was associated with deep rooting in upland field conditions. In addition, Lou et al. (2015) constructed a linkage

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map and performed QTL analysis in rice using 180 RILs and found that six QTLs located on chromosomes 1, 2, 4, 7, and 10 were associated RDR. In another study the RILs, derived from Bala 3 Azucena, were used to study root growth and water uptake in rice (Price et al., 2002). This study revealed that out of 24 genomic regions, seven QTLs on chromosomes 1, 2, 4, 7, 9, and 11 were reported to be crucial for root growth traits. DHLs, derived by crossing indica and japonica rice, were used to map 39 QTLs for traits associated with the morphology and distribution of roots (Yadav et al., 1997). Additional QTLs were reported for shoot biomass, deep root morphology, and root thickness by Kamoshita et al. (2002) and Champoux et al. (1995). Top soil layer is easily penetrated by plant root systems. However, top layer is vulnerable to short periods of drought. Therefore drought-resistant genotypes should access water from deep soil layer. Root penetration ability, through compact soil layer or hard pan, is a phenomenon in lowland rice fields. Several QTLs were mapped on rice chromosomes for RL, root number, root thickness, and root penetration index on hard pan (Ali et al., 2000; Zhang et al., 2001; Zheng et al., 2000). Differences in experimental conditions marked significant differences in consistency of identified QTLs for root traits (Kamoshita et al., 2002). Genotype-by-environmental interaction between greenhouse and field experiments were also observed (Champoux et al., 1995). Drought stress imposed artificially by polyethylene glycol in the hydroponics grown rice seedlings was utilized to identify QTLs for several root traits (Cui et al., 2008; Kato et al., 2008). The improved root morphological traits QTLs identified in the donor rice parent Azucena, an upland japonica ecotype, were introgressed into indica rice through MABC method (Steele et al., 2006). They found that an introgressed target segment containing QTL on chromosome 9 showed increased RL under both irrigated and drought conditions in indica rice. QTL analysis of cell membrane stability in plant species will be helpful to understand genetic factors influencing this trait. Tripathy et al. (2000) studied the genomic regions controlling QTLs for CMS in rice. In rice, 104 DHLs derived from CT99993 3 IR62266 were experimented by withholding water on 50-day-old seedlings. They found that nine QTLs were associated with CMS and individual QTLs explained up to 42.1% phenotypic variations. 38.2.1.5 Yield responses under drought Pulse crops such as chickpea (Cicer arietinum), lentil (Lens culinaris Medik.), pea (Pisum sativum L.), and bean (Phaseolus vulgaris L.) are major sources of dietary protein in the developing countries and frequently suffer from end of season or terminal drought. Ninety percent of chickpea growing areas depend on residual or conserved soil moisture (Upadhyaya et al., 2012). Therefore identification of drought tolerance QTLs in chickpea is critical. For this a mapping population was developed by crossing a drought-tolerant genotype ILC588 to a drought susceptible cultivar ILC3279. Fifteen genomic regions that were related to grain yield (GY) under terminal drought stress were identified (Rehman et al., 2011). In addition, Hamwieh et al. (2013) identified 93 QTLs across genome 3 environment interactions with the same mapping population. They suggested that the LG3 and LG4 had pleiotropic QTLs and could be targets to utilize molecular breeding for improving chickpea drought tolerance.

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Peanut (Arachis hypogea) is an allotetraploid (2n 5 4x 5 40) crop primarily grown for seed oil or as food (Bertioli et al., 2016; Peng et al., 2017). Since more than two-thirds of peanut is grown in rain-fed regions, drought is a major constraint, which limits the production of this crop. Ravi et al. (2011) identified 105 QTLs related to drought tolerance in groundnut utilizing a mapping population of TAG24 3 ICGV 86031 and classified them as main effect QTLs and epistatic QTLs due to the complexity of drought tolerance and interactions between genotype and environment effects. Faye et al. (2015) used the same mapping population and phenotyped them under different water regimes. They found 52 QTLs with low phenotypic variance, and some of the QTLs were colocalized with previous study of Ravi et al. (2011). From these experiments, they suggested that genomic selection would be a more appropriate approach to accumulate most of the minor-effect QTLs under elite genetic background than MAS or MABC program. In addition to grain crops, forage crop breeding is also utilizing molecular markers to locate QTLs, which is linked to biomass production under drought conditions. Alfalfa is a highly nutritious legume crop that has been used to feed livestock and improve soil quality by nitrogen fixation (Adhikari and Missaoui, 2017). However, due to the allogamous nature of this crop, severe inbreeding depression limits the ability to develop homozygous inbred lines for mapping population development (Gallais, 1984). A BC mapping population was developed between high-WUE, Medicago sativa subsp. falcata and low-WUE, M. sativa subsp. Sativa (Sledge et al., 2005). A total of 206 BC1 were evaluated for forage yield under seven water stress environments, and 10 and 15 QTLs were identified that were associated with improved and reduced forage biomass yield during drought stress, respectively (Ray et al., 2015).

38.2.2 Mineral stress Mineral stress is a critical abiotic stress that impacts the yield of crops. Each macromineral (N, P, K, Ca, Mg, and S) and micro-mineral (B, Fe, Mn, Zn, etc.) are required in right combinations to perform specific functions, grow, and reproduce (Loneragan, 1968). Inadequate amount of these nutrients express obvious and/or subtle symptoms. Supplying desired minerals, in the form of fertilizer, is not always feasible due to availability and marginal profitability. Some fertilizer source, such as phosphate rock reserves, is finite and nonrenewable (Li et al., 2014a). Besides, excessive use of fertilizer leads to groundwater pollution due to leaching, nitrification, and eutrophication (Savci, 2012). Although the plant nutrient in the soil is high, the presence of ferrum (Fe) and aluminum in acidic soils and that of calcium and magnesium in alkaline soils causes minerals to become fixed and become unavailable to plants (Geisseler and Miyao, 2016). Developing a specific mineral-efficient genotype requires an understanding of multiple interrelated traits into three broad mechanisms. First, a mineral must be available in the plant absorbable form (mineral interception). Second, root systems must uptake absorbable minerals in sufficient amount (mineral uptake efficiency) and load them into xylem system. Third, upon reaching the source, those minerals must be unloaded and transferred to the right cells (mineral utilization efficiency) (Wang et al., 2008). Common modification in response to low mineral stress includes change in root/shoot ratio, root architecture

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system, the induction of mineral transporters, secretion of organic acids by roots, biomass change, and yield and productivity change (Raghothama and Karthikeyan, 2005). Sufficient genotypic variation already exists for such traits in different crops to make it possible to breed for improved mineral deficiency tolerance. However, genetic basis and possible candidate genes for these traits are needed before they can be deployed in crop development. With few exceptions, most of the mineral deficiency tolerance traits have continuous phenotype distributions, that is, these traits are controlled by multiples genes (Doerge, 2002). Contrasting parents are required to detect QTLs, and as expected, many QTLs were not detected when Wu et al. (2008) constructed 183 DHLs using parents that were not contrasting for leaf mineral concentration. However, QTLs segregating for shoot dry biomass were detected in the same population. Majority of the QTL studies use secondary traits as a proxy to map QTLs related to the specific mineral deficiency. Very few studies mapped QTLs using primary traits itself. Nevertheless, alleles that decrease trait differences between stressed and normal conditions are critical in any crop improvement program (Cui et al., 2014). 38.2.2.1 Quantitative trait loci related to macro-minerals Many QTLs related to macro-minerals have been identified in various crops. 38.2.2.1.1 Nitrogen deficiency quantitative trait loci

Nitrogen is absorbed by plants in ammonium (NH41) and nitrate (NO32) form from the soil (Hofman and Van Cleemput, 2004). Typical nitrogen-stressed plants will show lower leaves lighter than upper without much leaf drop. Besides yield, low N (LN) significantly reduced end-use quality traits in wheat (Cui et al., 2016) and altered root morphology and nitrogen use efficiency (NUE) in maize (Li et al., 2015a; Kindu et al., 2014). In a study using agronomic traits, 12 constitutive QTLs were detected in both low and high nitrogen conditions, whereas seven and eight environment-specific QTLs were detected in each of these conditions, respectively (Kindu et al., 2014). NUE, a complex trait with moderately high heritability, is a combination of nitrogen uptake efficiency (NupE) and nitrogen utilization efficiency (NutE) (Kindu et al., 2014). Fifteen QTLs related to NUE were detected at LN on chromosome 3H, 5H, and 2H in barely (Kindu et al., 2014). N recycling or its regulatory genes were located as the candidate genes of those 15 QTLs in 3H and 6H. In a study by Cassan et al. (2010), nearly 70% of the NUE-related QTLs were associated with root system architecture (RSA) QTLs, most of which explained less than 20% phenotypic variation. In the stressed environment, 14.8% 15.9% mean GY increase was obtained by incorporating this NUE QTL. NupE had a significant phenotypic correlation with RSA than NutE (Cassan et al., 2010; Li et al., 2015a). Therefore under optimum nitrogen conditions, the accumulation of nitrogen reserves increases in plant and less mobilization occurs (Cassan et al., 2010). LN reduces the number of crown roots but increases the total length in maize (Li et al., 2015a). Rice adapts to LN stress by increasing root weight and length. Location of relative RL (RRL) QTLs mapped to similar location of NADH-dependent glutamate synthase (NADH-GOGAT) that controlled N recycling in rice chromosome 1 (Feng et al., 2010). QTLs for relative plant weight (rpw1a) and relative shoot weight (rsw1a) were located on loci of NADH-GOGAT on chromosome 1 in rice (Lian et al., 2005). Root weight

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QTL (n-r3) and relative shoot weight QTL (rswb3) corresponded to the location of GS1 and GDH2 gene location on chromosome 3 based on functional marker analysis (Lian et al., 2005). Extensive work has been done in identifying QTLs related to nitrogen stress in wheat. Rht-B1 locus for plant height on chromosome 4B and Ppd1 locus for photoperiodism on 2D1 alters the adaptation of wheat-to-nitrogen stress (Cui et al., 2016; Laperche et al., 2008). Mapping nitrogen nutrition index as a ratio of N content to critical N content in vegetative parts, 14 QTLs on 4B, and seven QTLs on 2D1 were identified that were close to markers rht-b1 and gpw4085, respectively. The former is markers linked for Rht-B1 gene and later is for Ppd1 locus. At Rht-B1 locus, dwarf alleles (Rht-B1b and Rht-B1c) increased kernel number (KN) and plant sensitivity to N stress in LN and at the Ppd1, late allele increased KN under LN. Dwarf lines remobilized nitrogen less efficiently than tall lines (Laperche et al., 2008). Rht-B1b, with Xmag4087 markers, enhanced the tolerance of test weight, kernel weight (KW), and thousand KW (TKW) in N stress conditions. Indirect selection for TKW maximized genetic gain for improving N stress tolerance (Cui et al., 2016). Marker Xmag4087 was the closest marker for grain protein content and wet gluten content QTLs QGpcdv-4B, QGpc-4B, QWgcdv-4B, QWgc-4B on chromosome 4B. The PinbD1b, allele on Pinb-D1 gene for grain hardness on chromosome 5D, improved the tolerance of kernel hardness, water absorption in LN conditions. Marker Xcfd18 was associated with QTLs QAbsdv-5D, QAbs-5D, QKhdv-5D, QKh-5D. As expected for most of the polygenic traits, a larger portion of phenotypic variation explained for nitrogen stress induced QTLs were explained by QTL-by-QTL interaction effects and very little from QTL-byenvironment interactions (Lian et al., 2005). 38.2.2.1.2 Phosphorus deficiency quantitative trait loci

Absolute and relative traits were studied to understand genetic basis of P stress tolerance in rapeseed (B. napus) (Ding et al., 2012), common beans (P. vulgaris L.) (Liao et al., 2004), soybeans (Zhang et al., 2016b), maize (Qiu et al., 2013), rice (Zhang et al., 2018b), and wheat (Zhang and Wang, 2015). Multiple root-related traits are frequently studied in response to varying P condition, namely, RL (Reymond et al., 2006), root angle (Liao et al., 2004), and root exudation (Hu et al., 2001). Genotypes with shallow root significantly increased shoot biomass and P uptake (PUP) (Liao et al., 2004). Similarly, genotypes that were P-efficient had longer and denser hairs (Yan et al., 2004; Zhu et al., 2005). A major QTL for primary root response to low phosphorus (LP), LPR1, at 2.8 Mb region on chromosome 1, reduced primary RL and promoted shallow root in mouse ear cress (Arabidopsis thaliana) (Reymond et al., 2006). Three LP-specific unique QTLs, uq.A1, uq.C3a, and uq.C3b were identified in rapeseed. QTLs uq.C3a, with the closest functional marker BnIPS2-C3 linked to gene AT4, was related to lateral root development and PUP. QTL uq. c3b, flanked by BnGTP1-C3, was related to gene AtGPT1 that translocates P from root to shoot and utilizes P (Yang et al., 2010). Of 62 significant QTLs detected, 26 QTLs were identified in only one environment, and the remaining 36 QTLs were detected in at least two environments representing sQTL. Analysis of variance suggested that those 26 environment-specific QTLs were environmentally influenced (Yang et al., 2010). Shoot phosphorus use efficiency (PUE), whole plant PUE, and acid phosphatase activity (APA) in maize was studied in an F2:3 population derived from a cross between 082 and Ye107 (Chen et al., 2009; Qiu et al., 2014, 2013). QTLs for APA in root (APR) and

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rhizosphere soil (APS) were not only detected in both environments, but also in the joint analysis of both environments (Qiu et al., 2014). One cQTL for shoot PUE and whole plant PUE was identified on chromosome 10 flanked by bnlg1518 bnlg1526 (Chen et al., 2009). QTL AP9 for APA in plant leaf on chromosome 9, flanked by umc1743 umc2398, was stably expressed in the different environments. Eventually, QTL AP9 was fine mapped to 540 kb region flanked by markers ac219 ac2096 in BC inbred line (BIL) (Qiu et al., 2013). After introgression, this QTL increased APA production by 18.35%. Qiu et al. (2014) also found three QTLs for APR and APS in the same F2:3 population. Twenty and fourteen environment-specific QTLs were detected under LP and normal phosphorus conditions, respectively, in soybean (Zhang et al., 2009). A novel environment-specific QTL, q13-2 expression was induced by low P stress on chromosome 13 in soybean (Zhang et al., 2016b). Relationship of PUE traits with different aspects of root traits was studied in the RIL of beans created by crossing DOR364 and G199833 (Beebe et al., 2006; Lian et al., 2005; Liao et al., 2004). Liao et al. (2004) found three QTLs for basal root growth angle, and shallow basal RL were closely linked to QTLs for phosphorus uptake efficiency (PupE) (Rsb4.1/ Pup4.1, Rsb7.1/Pup7.1, Sbr11.1/Pup11.1). Three of the root-exudation QTLs (Tae4.1, Hex4.1, and Hex10.1) were closely linked with QTLs for PUP (Pup4.1, Pup10.1) in the same RIL population in the field (Yan et al., 2004). The association of Pup4.1 with RL QTLs identified on linkage group (LG) B4 for both high phosphorus and low phosphorus environments suggests that longer rooting systems is important for P accumulation (Beebe et al., 2006). In rice, one major QTL for phosphorus uptake (Pup1) was identified that was closely linked to marker C443 C2140 flanking 13.2 cM region at 54.5 cM on the long arm of chromosome 12. One minor QTL linked to marker C498 on chromosome 6 was also identified (Wissuwa and Ae, 2001). These QTLs increased PUP by 3 4 and 0.6 0.9 times, respectively, by maintaining higher root growth rates. Wissuwa et al. (2002) developed NIL-derived F2:3 population to fine map Pup1 to 3 cM region. Substitution mapping revealed that Pup1 is cosegregated with marker S13126. The occurrence of three QTLs clusters for root traits and P efficiency at low phosphorus condition indicates that root traits contribute more to P efficiency under P stress (Liang et al., 2010). Phosphorus-related QTLs often coincided with those for root-related traits (Beebe et al., 2006; Luo et al., 2017; Shimizu et al., 2004). Therefore root-related traits are logical selection parameters to identify P-efficient genotypes. Zhang et al. (2010, 2009) repeatedly identified a QTL linked with marker Satt274 on the D1b 1 W chromosome with the use of same RIL population in soybean (Glycine max). A consistent QTL for P efficiency between linkage and association analysis, qPE8, on chromosome A2 was narrowed down to 3.3 cM that corresponded to 700 kb region. Eventually, GmACP1, gene underlying qPE8, flanked by marker 2645532 marker 2634911 was cloned (Zhang et al., 2016b, 2014a). In the same study a highly significant novel QTL, q4-2 on chromosome C2 was consistently detected regardless of traits, years, and treatment. This QTL is presumed to be controlled by Glyma.04214000 genes that encode pectin methylesterase (Zhang et al., 2016b). QTLs for tolerance to P deficiency (TPDE) on rice tends to cluster on chromosome 4, 6, 10, and 11 (Zhang et al., 2010). Three QTLs qTPDE4, qTPDE10, and qTPED11.3 were identified by using a RIL population from the cross of XieqingzaoB and DWR. The effect of QTL qTPDE4 on chromosome 4 was maximum and the effect and locations of these QTLs were

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validated using NIL. PupE was negatively correlated with PUE (Guo et al., 2017; Su et al., 2006). However, Su et al. (2006, 2009) observed positive linkage between phosphorus utilization efficiency (PutE) and PUP at three loci on chromosome 2D, 3A, and 3B flanked by Xgwm157 Xgmw539 and P8422-170-CWM539.2, and P2076-147-Xgwm108, respectively, that suggests the possibility of simultaneous improvement of PUP and PutE. Yield and biomass traits are often used as a proxy for P efficiency traits (Koide et al., 2013). Three sQTL clusters were detected on maize chromosome 1, 5, and, 10, respectively, for GY and yield-related traits in different P conditions (Li et al., 2010). In an association analysis, marker PgPb7101 was linked with increased P concentration in stover, increased P in total biomass, reduced PutE, and increased GY (Gemenet et al., 2015) in high phosphorus condition. Two sQTL clusters for biomass, PUE, and P acquisition efficiency-related traits were identified on chromosome 3H in barley (Hordeum vulgare) (Guo et al., 2017). Two significant QTLs identified for early vigor in wheat on chromosome 4B and 4D were underlined by Rht-B1b and Rht-D1b, respectively, both of which confer semidwarf phenotypes (Ryan et al., 2015). Rht-B1b and Rht-B1c alleles significantly reduced shoot biomass and RL compared to Rht-B1a allele, irrespective of P levels. Zhang and Wang (2015) detected QTL QRUP for root phosphorus uptake on chromosome 4B in different populations with multiple P levels. Chromosome 5A appeared as a major locus for PUP regulation at the seedling stage (Su et al., 2009). Two QTL clusters for tiller number and shoot dry weight on chromosome 5A were closely linked with vernalization requirement genes VRN-A1 on chromosome 5A and VRN-D1 on chromosome 5D. VRN genes have also been found to impact morphological traits such as tiller number in addition to flowering time (Su et al., 2006). Most significant QTL for APA in maize in low phosphorus condition, AP9 was detected in F2:3 families. This QTL represented 17 Mb genomic region according to B73 reference physical map. Two BIL populations were developed to fine map AP9 to a reasonably shorter region. First BIL narrowed down the QTL region to 3.5 Mb size, and second BIL limited the region to a 0.54 Mb region with 24 possible candidate genes (Qiu et al., 2013). QTL for phosphorus efficiency on chromosome 8, qPE8 in soybean was mapped by linkage mapping. This QTL was narrowed down to 250 kb region flanked by Sat_233-BARC039899-07506. With the help of plant transformation and regional candidate gene approach, GmACP1 was confirmed as candidate gene controlling qPE8 QTL (Zhang et al., 2014a). A major QTL for phosphorus uptake Pup1 was identified on chromosome 12 flanked by C449-G124A, a 13.2 cM region in BC1F6 population. This region was narrowed down to 3 cM flanked by S14025 S13126 with BC4F2:3 population. Zhang et al. (2018b) detected three QTLs in rice for TPDE, qTPED4, qTPDE10, and qTPDE11.3 using RIL and validated three QTLs using RIL-derived NIL (BC4F4). QTL qTPDE4 was most stable against P deficiency in both RILs and NIL. Mixed linear model approach was used to identify three markers associated with iron deficiency chlorosis (IDC) in an AM population. Among these, two markers, Satt114 and Satt239, were confirmed in a second AM population (Wang et al., 2008). 38.2.2.1.3 Potassium deficiency quantitative trait loci

Potassium is absorbed as potassium ion (K1) form (Maathuis and Sanders, 1996). Yellowing at leaf margins continuing towards the center is a typical K deficiency symptom (Marr, 1994). However, K deficiency does not show immediate symptoms. Potassium

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deficiency decreased most of the biomass-related traits and K content traits; however, Kuse efficiency and a ratio of seedling root dry weight to seedling shoot dry weight were increased. With the use of nutrient-use index, ratio of biomass to tissue nutrient concentration), over 100 QTLs for low K were identified in hydroponics, pot, and field trials (Kong et al., 2013). Fifteen relatively high-frequency QTLs, which were detected in more than 50% of the treatments, were identified. A total of 21 cQTL mapped 56.9% of the total QTLs identified onto 13 chromosomes. These 21 cQTL were growth stage-dependent. 38.2.2.2 Quantitative trait loci related to micro-nutrients About half of the world’s soils are deficient in micronutrient (Baligar et al., 2001) that stresses the need to develop new varieties that can maintain both higher yields and nutrient use efficiency. 38.2.2.2.1 Iron (Fe) deficiency quantitative trait loci

Iron is a major constituent of ferredoxin, an element required for chlorophyll formation (Boardman, 1975). In low iron conditions, chlorophyll production is reduced, as characterized by interveinal chlorosis. In mung bean (Vigna radiata), iron deficiency tolerance was assumed to be controlled by a single dominant gene (Srinives et al., 2010). The authors detected a major QTL controlling resistance to IDC, qIR (R2 5 76.39%) at 26.4 cM flanked by amplified fragment length polymorphism (AFLP) markers E-ACT/M-CTA and EACC/M-CTG on chromosome 3 in mung bean (Srinives et al., 2010). However, with the same F2:4 population, Prathet et al. (2012) showed it to be controlled by a major QTL with other modifying genes. Prathet et al. (2012) detected two QTLs for IDC trait, qIDC3.1 (R2 5 41.67%) and qIDC2.1 (R2 5 45.66%) on chromosome 3 and 2, respectively. The robust, stable, and major QTL qIDC3.1, flanked by simple sequence repeat (SSR) CEDG084 and CEDC031 at 126.9 cM on chromosome 3, was the same as qIR from the previous study (Prathet et al., 2012; Srinives et al., 2010). However, those two markers were dominant in nature and were 3.1 cM and 10 cM far from qIR, respectively, making these markers not amenable to MAS (Srinives et al., 2010). Markers from Srinives et al. (2010) also flanked the qIDC3.1; therefore they have same mechanisms of resistance to IDC. The other QTL qIDC2.1 was presumed to be the modifier of qIDC3.1 and environmentally sensitive. Presence of up to six QTLs for an iron deficiency trait in grapes (Vitis vinifera) further supported the above statement that this trait is under polygenic control (Bert et al., 2013). A QTL cluster for chlorotic symptoms (R2 5 10% 25%), chlorophyll content (R2 5 22%) and plant development (R2 5 50%) was identified on chromosome 10 in grapes (Bert et al., 2013). QTL for ferric reductase activity and shoot chlorosis SPAD value colocalized at 94.8 cM on chromosome 3 with TM0213 as a linked marker (Klein et al., 2012). This QTL was mapped into the same region as ferric reductase gene LjFRO1 since TM0213 flanked both the gene and the QTL. From the amino acid sequence alignment, minor amino acid sequence differences were observed between parents on LjFRO1 region. Using the same population, One major gene on chromosome N and modifying QTL on LG A1 and L were identified for IDC in F2:4 ankora and pride soybean population (Lin et al., 2000a, 2000b). IDC was controlled by multiple genes in pride population. However, in ankora population, the trait was controlled by a major gene on LG N explaining 72.7% of the phenotypic

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variation. This QTL was common in both mapping populations. Two markers Satt114 and Satt239 in the two AM populations were associated with IDC (Wang et al., 2008). 38.2.2.2.2 Manganese deficiency quantitative trait loci

Chloroplast is very sensitive to Mn deficiency (Qu et al., 2012). Therefore, manganese deficient leaves appear netted because chloroplast doesn’t work properly and only the small veins remain green in color. A locus for Mn efficiency, Mel1I (R2 5 69%) on chromosome 4HS with flanking marker Xabg714 was detected in barley. This QTL also explained 65% of the phenotypic variation for shoot Mn concentration. Another marker Xcdo583B, 3.4 cM away from Mn efficient loci Xabg714, explained 67% of the variation for shoot Mn concentration. A goodness of fit analysis of marker selected F4 progeny revealed Mel1 as a major QTL with other additional minor QTLs involvement (Pallotta et al., 2000). In durum wheat (Triticum turgidum), a QTL for shoot Mn concentration (R2 5 42%) was detected on chromosome 4B with linked marker Xcdo583a. Comparing observed and expected variance indicated this trait as a two-locus model. Markers from Pallotta et al. (2000) were exploited to map in this population. Several loci associated with Mn efficiency in both barley and durum wheat were also identified (Xcdo669/HindIII, Xwg622/HindIII and Xcdo583a/HindIII) (Khabaz-Saberi et al., 2002). In barley, Mn efficiency locus, Mel1, identified on chromosome 4HS, was identified using bulked segregant analysis (BSA) of F2 plants. Association of Mel1 and Markers Xcdo583B and Xabg714 were confirmed with F2 population and DHLs derived from the same parents. Locus Mel1 was further confirmed in field using MAS of F2:4 lines from the same population (Pallotta et al., 2000). 38.2.2.2.3 Boron deficiency quantitative trait loci

Boron (B) is an important element for ovary and pollen development with its deficiency resulting in a significant loss of seed viability and seed yield (Rerkasem, 1996). A major, dominant gene for B-efficiency, BE1, was detected on LG 9 flanked by pa28c and tg2h10b at 0.8 and 6.6 cM, respectively, on rapeseed (Xu et al., 2001). This QTL was overlapped by two QTLs for bolting date and two QTLs for maturity date. This implies that these traits could be controlled by pleiotropic effects of single genes or due to tight linkage of several genes. Boron efficiency coefficient (BEC) in A. thaliana was governed by at least four QTLs, AtBE1-1, AtBE1-2, AtBE2, and AtBE5, with most of them explaining more than 10% of the variation. Three QTLs, AtBE1-2, AtBE2, and AtBE5, were detected in both the RIL and F2 population used at the same peak position and these QTLs had a large effect on BEC (Zeng et al., 2008). AtBE1-2 (R2 5 23.8%) was responsible in utilization and/or distribution of B to the silique in low B condition (Zeng et al., 2007). Three QTLs for seed yield at low B were also detected at the interval of the corresponding QTLs for BEC in both the populations. The locus of AtBE1-2 was validated by joint analysis of RIL and F2 populations. QTL BE1 identified in Xu et al. (2001) overlapped with AtBE1-2 (Zhang et al., 2001). QTL AtBE1-2 identified for boron efficiency using conventional/unconditional QTL mapping was confirmed using conditional mapping. This QTL was also verified using an F2 population developed by crossing a B-efficient RIL with a B-inefficient RIL (Zeng et al., 2008).

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38.2.2.2.4 Zinc deficiency quantitative trait loci

Characteristic symptoms of Zn deficiency in rice are brown blotches and streaks on leaves that cover entire leaves later (Yoshida et al., 1973). Zn deficiency tolerance is governed by several medium and small effect QTLs (Lee et al., 2017). Five macro-minerals (N, P, K, Ca, Mg), four micro-minerals (Fe, Zn, Mn, Cu), Sr, and Al were studied under Zn deficient condition in field mustard (Brassica rapa). Significant correlations were found, but not many QTLs were colocalized since many QTLs with minor effects that governed mineral accumulation could not be detected (Wu et al., 2008). Three important QTLs for leaf mortality and leaf bronzing in Zn deficient conditions were detected on chromosome 1, 2, and 12 in rice each explaining 10.9% 16.5% and 11.8% 24.2% of the total variation in hydroponics and field experiments. Only two QTLs associated with leaf bronzing were associated with plant mortality, Zbz1b/Zmt1 and Zbz7/Zmt7 (Wissuwa et al., 2006). By combining biparental and genome-wide association (GWA) studies (GWAS) data, three QTLs were colocalized for root, biomass, and yield traits on chromosomes 3, 6, and 12 in rice (Lee et al., 2017). In both analyses a QTL located at 26 28.5 Mb on chromosome controlled four traits. From transcription data, one candidate gene, Os60g44220, was identified in chromosome 6 and was annotated as a putative low temperature and salt responsive protein. Haplotype analysis revealed four base pair change between parents in the promoter region of this candidate gene (Lee et al., 2017).

38.2.3 Mineral toxicity Plants absorb nutrients in ionic form with the root system via diffusion or mass flow from the soil (Epstein and Hagen, 1952). Though minerals are required by plants for normal growth and development, these minerals can be toxic at higher concentrations (Garbisu and Alkorta, 2003). Higher concentrations of minerals result in overproduction of reactive oxygen species and hydrogen peroxide (H2O2) ultimately causing poor root growth, damage of photosynthetic pigments, and reduced chlorophyll level, thereby causing poor growth and reducing the overall yield of plants (Krupa, 1988; Landi et al., 2013; Stobart et al., 1985). The best way to cope with mineral toxicity is to identify the QTLs and genes related to mineral toxicity and increasing the mineral stress tolerance from available germplasm. 38.2.3.1 Aluminum Aluminum (Al) is soluble in acidic soil and becomes readily available for uptake by plant roots (Sumner et al., 1991). The root tips are highly sensitive to Al toxicity that inhibits cell division and cell elongation and negatively impacts the growth and development of roots. The poor root growth will ultimately affect shoot growth and development (Ryan et al., 1993; Sivaguru and Paliwal, 1993). The acidity of soil can be minimized by the application of lime, but still, the subsoil remains acidic and Al toxicity limits the growth of roots, thereby causing drought stress (Caires et al., 2008). The first Al-tolerant mutants in A. thaliana were identified in ecotype Columbia (Col-0) by treating seeds with mutagenic chemical, ethyl methyl sulfonate and staining the roots of the mutant population with morin (Larsen et al., 1996). Later, genetic analysis of those mutants identified that the Al

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resistance was semidominant, and random amplified polymorphic DNA (RAPD) markers showed that mutants mapped to two loci in different chromosomes. One locus was mapped to chromosome 1 and the other to chromosome 4 (Larsen et al., 1998). Kobayashi and Koyama (2002) analyzed 100 RIL obtained by crossing Landsberg erecta (Ler-0) with Col-4. They identified Al-tolerant lines on the basis of RL at toxicity of 4 μM of AlCl3 and pH 5. By using RRL, single factor QTLs were identified in chromosome 1 and 4, while by using complete pairwise search method, five epistatic loci pairs were identified (Kobayashi and Koyama, 2002). The key trait behind Al tolerance is the release of Al binding organic acids from the root tips after Al toxicity in root area. Hoekenga et al. (2003) also studied 100 recombinant inbred (RI) populations obtained by crossing Ler-0 with Col4 and found two QTLs cosegregating with the release of malic acids from the roots after Al toxicity. Similarly, two QTLs were linked to the same chromosomal position in Col/ Kashmir RI populations by using SSR and cleaved amplified polymorphic sequence (CAPS) markers (Ikka et al., 2008). In alfalfa, callus growth bioassay and RFLP markers were used for QTL identification that were associated with Al tolerance in coerulea subspecies. QTLs identified in tissue culture were highly associated with the QTLs identified from RFLP markers, and so far two RFLP markers (UGAc4 and UGAc502) in F2 and BC populations were identified (Sledge et al., 2002). Later, SSR markers were used to verify and flank the two QTLs identified, and EST-SSR markers were used to construct genetic linkage map (Narasimhamoorthy et al., 2007). Using expressed sequence tags (ESTs) that were homologous to identified QTLs in other crops, six candidate gene markers were identified. Similar technique was followed in the segregating population obtained from the cross of Al-tolerant (Altet-4) and Al-sensitive (NECS-141) genotypes and the linkage map covered 761 and 721 cM, respectively (Khu et al., 2013). Alp gene in barley cultivars Dayton confer tolerance to Al toxicity and hence F2 mapping population of Dayton/Harlin were analyzed for RFLP mapping of Alp gene which was linked to Xcdo1395 marker (Tang et al., 2000). F2 and F3 population from the cross of medium Al-tolerant and Al-tolerant genotypes were studied with AFLP and microsatellite markers to identify a single major gene, Alt governing Al tolerance (Raman et al., 2002). Similarly, RFLP and AFLP were employed in wheat RILs for identification of markers linked with aluminum tolerance (Ma et al., 2006; Riede and Anderson, 1996). Malate transporter gene related with Al tolerance on the distal region of 4DL chromosome was mapped by SSR markers (Cai et al., 2008; Ma et al., 2005). Later, in addition to major QTL on chromosome 4DL, another major QTL was mapped to 3BL chromosome by the use of SSR markers and root characteristics (root tolerance index and new root growth) in wheat (Dai et al., 2013; Navakode et al., 2009). Rye is the most Al-tolerant Triticeae species. In addition to two markers, three markers linked to Alt gene located on 3RL, 4RL, and 6RS genes were identified by employing AFLP and RFLP markers in F6 rye RIL populations (Miftahudin et al., 2002). Moreover, four QTLs were identified in oat by covering a larger area of the genome using AFLP and sequence characterized amplified region (SCAR) markers (Wight et al., 2006). Rice is the only cereal crop cultivated in water-logged conditions, and it shows tolerance to Al toxicity among small grain cereals. To identify the genetic mechanism behind Al tolerance in rice, Wu et al. (2000) studied RRL in RI population from a cross of

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Al-sensitive indica and Al-tolerant japonica rice with RFLP and AFLP markers. Based on segregation for RRL, linkage map was constructed with 103 RFLP and 104 AFLP markers which identified two QTLs on chromosomes 1 and 12 (Wu et al., 2000). Similarly, 183 BILs of cross between Al-tolerant japonica and Al-sensitive indica rice were investigated on the basis of Al-content in root apex and citrate secretion leading to the identification of three putative QTLs on chromosome 1, 2, and 6. QTLs on chromosome 1 and 2 reduced Al tolerance while QTL on chromosome 6 increased Al tolerance (Ma et al., 2002). Moreover, in another cross of japonica and indica rice, three QTLs were mapped to chromosome 1, 9, and 11 based on relative root elongation (Xue et al., 2006). Al-susceptible and Al-tolerant indica rice were crossed, and their F3-selfed progeny were analyzed for relative root growth by using RFLP markers to construct a map with 164 loci covering most of the rice genome (Nguyen et al., 2001). The highest effect of aluminum tolerance was mapped to chromosome 1 which did not correspond with other genes that were mapped for Al tolerance mapped in other crops; hence, they suggested that Al tolerance could be best explained as polygenic trait. In 2014, Xia et al. (2014) identified Nrat1 gene by studying chromosome substitution lines. Recently, SSR markers were used for AM and Al tolerance in 150 accessions of rice landraces identifying 23 associations of which 3 were identical to previously reported QTLs and 20 were new associations (Zhang et al., 2016a). 55K rice single nucleotide polymorphisms (SNP) array was used in rice multiparent advanced generation intercross populations and 21, 30, and 21 QTLs for Al, Zn, and Fe stress tolerance, respectively, were identified (Meng et al., 2017). In soybean, 120 F4-populations obtained by crossing Young with PI 416937 were examined under Al-stressed condition for tap root elongation by using RFLP markers. Two RFLP markers linked to Al tolerance were detected from Al-tolerant parent PI 416937 (Bianchi-Hall et al., 2000). Later, SSR markers were employed to increase the power of QTL detection. Two major QTLs, qAL_HIAL_08 and qAL_PC_08, were mapped to chromosome 8 that explained 45% and 41% of variation, respectively (Abdel-Haleem et al., 2014). RL, root tolerance index, and relative mean growth of RILs from a cross of Essex/ Forrest were studied to identify Al-tolerant traits linked to two QTLs that explained 31% and 34% of the trait variation that were also responsible for citrate metabolism (Sharma et al., 2011). 38.2.3.2 Cadmium Cadmium (Cd) is a heavy metal that does not have any biological function in plants. They are highly toxic to plants and damage photosynthetic units and reduces the level of chloroplast in leaves, ultimately reducing plant biomass (Krupa, 1988; Moya et al., 1993; Padmaja et al., 1990; Stobart et al., 1985). For cadmium tolerance in Arabidopsis, RRL was studied as tolerance index in RIL population derived by crossing Ler-0 with Col-4 for identifying QTLs and epistasis related with cadmium tolerance. Three major QTLs on chromosomes 2, 4, and 5 were identified and the chromosome 5 QTL (QTL5) with the highest LOD score of 5.6 was able to explain 26% of the Cd tolerance variation (Tazib et al., 2009). SSR markers were used to identify Cd tolerance and genetic diversity in 120 bermudagrass accessions. This led to identification of 31 SSR markers associated with Cd tolerance which could be used for improving bermudagrass for enhanced Cd stress tolerance (Xie et al., 2015). In rice, DH population, derived by crossing japonica and indica rice,

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was studied for Cd tolerance. Under Cd stressed condition, three QTLs controlling Cd concentration were identified on chromosome 6 and 7, while one QTL for Cd ratio in shoot and root was mapped to chromosome 3 (Xue et al., 2009a). Apart from crop and model plants, Cadmium toxicity has been studied in Populus tree. Based on root volume and total dry weight, more than 16 QTLs with higher LOD score ( . 2.5) were identified which explained the phenotypic variation from 5.9% to 11.6% (Induri et al., 2012). 38.2.3.3 Selenium Selenium (Se) is essential to plants because active sites of some enzymes contain selenocysteine amino acid (Stadtman, 1990). Chemically, selenium is similar to sulfur, so nonspecific replacement of selenium with sulfur could lead to selenium toxicity in plants (Anderson, 1993). In A. thaliana, three Arabidopsis accessions Ler, Col, Wassilewskija (Ws) and their F1 and F2 populations were analyzed for selenium tolerance (Zhang et al., 2006a). Multiple genes responsible for selenite tolerance were identified and one major gene was accountable for tolerance to selenite. BSA of those F2 populations identified that the three molecular markers on chromosome 1, 3, and 5 (nga111, ciw4, and ciw8) were associated with selenate (Na2O4Se) tolerance, while a single marker on chromosome 4 was responsible for selenite tolerance (Zhang et al., 2006a). Later, RILs from a cross of Ler-0/ Col-4 was used for evaluating selenium tolerance index under selenium-stressed conditions, and three QTLs were mapped to chromosomes 1, 3, and 5 (Zhang et al., 2006b). 38.2.3.4 Boron Boron (B) is an important plant micro-nutrient, but it could be toxic to the plants if present at higher concentration in soil. Boron toxicity becomes more severe in dry soil where there is no or very low rainfall (Cartwright et al., 1984). The genetic variation of B tolerance was studied in many wheat and barley genotypes (Nable et al., 1997). DH wheat generated from a cross of B tolerant and moderately sensitive cultivars, was studied with both RFLP and AFLP markers, and two different loci on chromosomes 7B and 7D were found to be associated with leaf symptom expression for B toxicity (Jefferies et al., 2000). Boron transporter gene (Bot1) identical to boron tolerance QTL mapped to 6H chromosome was identified in DH barley population by using suppression subtractive hybridization technique (Hassan et al., 2010). The identification of two QTLs for germanium (Ge) toxicity were colocated with previously identified two QTLs for B toxicity located in chromosomes 6H and 2H (Hayes et al., 2013). Japonica rice genotypes were more tolerant to B than indica genotypes. A RIL population derived by crossing japonica and indica were studied for B tolerance and a major QTL for B tolerance was identified on chromosome 4 that explained 45% of the phenotypic variation (Ochiai et al., 2008). 38.2.3.5 Iron Iron (Fe) toxicity is very common in lowland rice. Due to continuous flooding and anaerobic condition, ferric iron reduces to ferrous iron which easily solubilizes in water and is readily available for uptake by plants (Gross et al., 2003). Presence of higher concentration of ferrous ion leads to peroxidation of plant lipids, degradation of proteins, inactivation of enzymes, bleaching of the photosynthetic pigments, and damaging of the chloroplast DNA (Bode et al., 1995). Iron toxicity tolerance in rice was studied in 164 RILs

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populations obtained from a cross of Azucena/IR64, which led the identification of 24 putative QTLs. The putative QTLs were mapped to chromosome 1, 2, 3, 4, 7, and 11 for different morpho-physiological traits (Dufey et al., 2009). Later, the same population was studied under high ferrous iron environments in hydroponics on washed sand and in the field identifying total of 44 QTLs. Joint QTL analysis confirmed that only 9 QTLs out of 44 were found in the same or adjacent regions in the chromosomes. They also aimed at exploring Fe tolerance traits from African rice Oryza glaberrima and studied 220 BC3DHLs obtained from BC of O. sativa/O. glaberrima with O. sativa under iron stressed (250 mg/L of Fe21) condition (Dufey et al., 2012). They identified 28 QTLs for 11 morphophysiological traits in 18 specific chromosomal locations. By using single and joint composite mapping, seven QTLs were identified in new regions of chromosome 1, 5, and 10 which were transferred from O. glaberrima parent (Dufey et al., 2015). Two parents Nipponbare (japonica rice) and Kasalath (indica rice) along with their 96 BC1F9 mapping populations (Nipponbare/Kasalath//Nipponbare) were studied to identify QTLs for several traits such as tiller number, stem and root dry weight, and leaf bronzing index in iron stressed condition (Wan et al., 2003). They identified four QTLs mapped to chromosomes 1 and 3 at higher LOD score (3.17 7.03). 38.2.3.6 Chromium Chromium (Cr) metal has two stable forms, trivalent chromium Cr(III) and hexavalent chromium Cr(VI). Hexavalent form is more toxic and is found in the form of chromate 22 (CrO22 4 ) and dichromate (Cr2 O7 ) oxyanions (Becquer et al., 2003). Chromium is highly toxic to both plants and animals and it is nonessential to plants (Dixit et al., 2002). A DH population developed from indica rice (ZYQ8) and japonica rice (JX17) were analyzed for chromium tolerance, where few lines along with ZYQ8 parent were found to show higher Cr tolerance. Three QTLs associated with Cr accumulation in shoot, in roots, and root: shoot ratio were identified (Qiu et al., 2010). 38.2.3.7 Manganese Manganese (Mn) toxicity is a major factor determining crop production in acidic soils. Higher Mn concentration in soil can hinder the uptake and absorption of other essential minerals (Ca, Mg, Fe, and P) and also affect enzymatic and hormonal actions of plants (Clark, 1982; Epstein, 1961). Japonica rice (Azucena) and indica rice (IR1552) had different levels of Mn toxicity tolerance. Therefore Wang et al. (2002) studied 150 lines from F9 RIL populations derived from the cross of these two parents. Manganese toxicity index was studied on this population based on leaf necrotic brown spots and Mn concentration in the shoots with 207 markers covering all 12 chromosomes. From this study, eight QTLs for Mn tolerance were identified and six QTLs out of eight were found to be contributed from tolerant parent IR1552 (Wang et al., 2002). Similarly, in soybean, RIL population derived by crossing Essex with Forrest genotypes were studied using RAPD and SSR markers (Kassem et al., 2004). The identified QTLs on chromosomal regions were significantly associated with root necrosis trait. Thus, Mn toxicity tolerance is a quantitative trait and is governed by multiple genes with different magnitudes of effect.

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38.2.3.8 Zinc Zinc (Zn) is an essential micro-nutrient required for plant growth and development. Both deficiency and excess of Zn concentration is harmful for plants, and Zn toxicity mostly occurs on acidic soils (Obata, 1995). In rice, RI population obtained by crossing Zn21 toxicity tolerant japonica variety and relatively Zn21 susceptible indica variety were studied for mapping of QTLs for Zn toxicity tolerance by using 289 RFLP markers (Dong et al., 2006). Three different QTLs for Zn21 toxicity tolerance were mapped to Chromosomes 1, 3, and 10 explaining 21.9%, 8.9%, and 7.6% of the variability, respectively. The damage index score due to Zn toxicity was continuous, and transgressive segregants of the index score suggests that the Zn21 toxicity trait is also a quantitative trait and is governed by multiple QTLs. 38.2.3.9 Copper Copper (Cu) is also one of the important micro-nutrients required for plants, and at the same time, higher concentration of Cu in the soil could be phytotoxic (Lanaras et al., 1993). For Cu toxicity tolerance, wheat was grown in control and Cu-stressed soil to identify QTLs related to Cu tolerance. One major QTL on chromosome 5DS and five minor QTLs on chromosomes 1AL, 2DS, 4AL, 5BL, and 7DS were identified (Ba´lint et al., 2007).

38.2.4 Heat stress Heat stress compromises crop yield and prolonged stress, or higher magnitude of stress can lead to complete crop failure. Cereals such as wheat and rice yield are affected by postanthesis heat stress (Yang et al., 2002; Tazib et al., 2015). High-resolution mapping uses SNPs from a 5K SNP array and a rice RIL population detected one major QTL, which could explain phenotypic variation up to 21% (Ps et al., 2017). QTL analysis of wheat F2 population directed to the identification of two linked markers with QTL of grain-filling duration (GFD) (Yang et al., 2002). More than 10 QTLs were detected for heat susceptibility index (HSI) of wheat yield components under short-time heat treatment upon grainfilling stage (Mason et al., 2010), while the QTLs related to HSI of GFD, yield components, and late-sowing were also detected on chromosomes 1B, 2B, 3B, 5A, and 6B (Sharma et al., 2016). Three major wheat QTLs for HSI, canopy temperature depression (TD), and latesowing were detected using RILs (Sharma et al., 2016). Similarly, seven loci for HSI and 22 QTLs for GFD, canopy temperature (CT), GY, and thousand grain weight using DH population were detected in hexaploid wheat (Tiwari et al., 2013). Genomic regions for wheat traits: grain quality after terminal heat stress (Beecher et al., 2012), HSI, and TD (Esten Mason et al., 2011) were identified in RIL population. Family-based mapping approach conducted in 19 wheat families of T. turgidum L. enabled the detection of heat stress QTL for chlorophyll content, KW, and flag leaf TD (Ali et al., 2013). BILs developed by crossing Aegilops speltoides and Triticum durum seemed useful to transfer heat tolerance features of A. speltoides to T. durum (Awlachew et al., 2016). QTL mapping performed for parameters of chlorophyll fluorescence kinetics (PCFKs) of wheat using DHLs displayed several QTL for the PCFKs (Azam et al., 2015). Three biparental wheat populations with genotyping

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information obtained using DArTseq and SSR genotyping permitted to identify loci for maximum quantum efficiency of photosystem II (Fv/Fm) (Sharma et al., 2017). Genetic control of heat tolerance in rice at anthesis was investigated via QTL mapping using RILs (F6) derived from Bala (tolerant) 3 Azucena (susceptible) cultivars, where eight loci for spikelet fertility at high-temperature condition were discovered (Jagadish et al., 2010). Of the eight loci, four QTLs were detected on the same genomic region where QTL for other stresses such as drought, cold, and salinity were identified, suggesting cross talk among abiotic stresses. Genomic loci for rice spikelet fertility at high temperature were detected using BC1F1 and F2 populations (Ye et al., 2012), whereas genetic loci for hightemperature tolerance in grain-filling stage of rice were investigated using RIL (Shirasawa et al., 2013). QTL mapping is performed for seed set trait in rice when flowering at hightemperature detected two major QTLs affecting seed set (Xiao et al., 2011). A genomic region in rice chromosome 4 that enhances spikelet fertility in high temperature at flowering stage were fine mapped previously (Ye et al., 2015), which narrowed down this QTL interval to 1.2 Mb. Possibility of using early morning flowering (EMF) from a wild rice Oryza officinalis to overcome the loss due to heat-induced spikelet sterility was investigated (Hirabayashi et al., 2015). An sQTL, qEMF3, detected using NILs could be useful to rescue rice flower spikelet from heat stress damage through the flower opening time manipulation (Hirabayashi et al., 2015). Genomic region controlling the basal dehiscence length in rice was detected using chromosome segment substitution lines, where the substitution lines were derived from rice cultivars 9311 3 Nipponbare (Zhao et al., 2016). Therefore, long basal dehisce in rice might be an important trait to improve heat tolerance. In crisphead lettuce (Lactuca sativa L.), heat stress related traits such as tip burn, rib discoloration, ribbiness, internal rib cracking, and premature bolting were mapped in 152 F7 RILs (Jenni et al., 2013). Genomic loci associated to seed germination and heterotrophic growth in Medicago truncatula under suboptimal and supraoptimal temperatures were studied in a RIL population that provided the putative candidate genes of M. truncatula for regulating seed germination at high temperature (Dias et al., 2011). The QTL and linked markers in cowpea for heat tolerance were identified in RILs derived from cowpea varieties CB27 and IT82E-18 (Lucas et al., 2013). Creeping bentgrass (Agrostis stolonifera L.) heat tolerance related traits such as turf quality, canopy TD, chlorophyll content, and membrane stability were investigated for the causal genomic positions in pseudo-F2 population (Jespersen et al., 2016). Broccoli (Brassica oleracea var. italica) heat tolerance QTL and epistasis interaction were identified using GBS markers in a DH population (Branham et al., 2017). Several heat stress responsive QTLs and putative candidate genes of chickpea have been reported using GBS SNPs and a RIL population (Paul et al., 2018). Since global warming has become a major issue and the rising temperature is a problem to be considered to protect flora and fauna of the earth, developing heat stress tolerant crop is ideal to feed the growing population.

38.2.5 Cold stress Cold stress impacts survivability, ecological distribution, and yield of the crops (Kreps et al., 2002). QTLs for cold tolerance have been mapped in several cereal, legume, forage,

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and horticultural crop species. QTLs for rice seed germination under low-temperatures were detected on rice chromosome 11 and chromosome 2 in a RILs derived by crossing japonica cultivar “Asominori” with indica cultivar “IR24” (Ji et al., 2009). Variable performance of rice RILs for cold tolerance at seedling stage (CTS) and low-temperature germinability (LTG) were used to detect relevant QTLs: qCTS8.1, qLTG11.1, qCTS11.1, qLDWcold10-1 that were mapped using multiple interval mapping methods (Wang et al., 2011a; Yang et al., 2017). Some cold-tolerant cultivars of rice are already available publicly. A cold-tolerant rice cultivar “Norin-PL8” was developed by introgression of QTL/genes on chromosome three and chromosome four from a cold-tolerant cultivar javanica (Saito et al., 2001). Fine mapping of the QTLs in the introgressed region of rice chromosome 4 in Norin-PL8 in NILs displayed two QTLs linked to cold tolerance, suggesting that introgression of causal QTL is an effective approach to improve the desired quantitative trait. Some QTLs and candidate genes for cold tolerance at booting stage were described previously in rice (Takeuchi et al., 2001; Kuroki et al., 2007; Zhou et al., 2010). One major rice QTL (qSCT-11) for cold tolerance during early seedling stage accounted 30% of phenotypic variation (Zhi-Hong et al., 2005), and the QTL was detected using RILs derived from single seed descent of japonica 3 indica cross. Different rice cold stress related QTLs, such as qCTS12 on chromosome 12 (Andaya and Tai, 2006), qSCT2 on chromosome 2 (Lou et al., 2007), and qCTS9 on chromosome 9, and other QTLs with medium effect have been reported (Pandit et al., 2017). QTLs for cold tolerance were also mapped using RILs developed by crossing a cold-tolerant rice “Geumobyeo” with cold-sensitive breeding line “IR66160-121-4-4-2” (Suh et al., 2012). Similarly, QTL mapping using rice RILs derived from Lijiangxintuanheigu 3 Sanhuangzhan-2 identified cold tolerance QTLs and other related QTLs for leaf yellowing, percent seedling survival, and leaf rolling (Zhang et al., 2014b). Liu et al. (2014) reported seven genomic positions associated to cold tolerance in a landrace rice “Xiang 743” at early seedling stage (Liu et al., 2015). They also detected five QTLs regulating cold tolerance in sensitive cultivars Katy and Dular using F2:3 lines. Fine mapping of two QTLs, qLOP2 and qPSR2-1, for cold tolerance in wild rice (Oryza rufipogon Griff.) seedlings in BC2F1 population and their introgression to chilling-sensitive rice cultivars (93-11 and Yuefeng) using MAS led to the development of improved rice cultivars for cold stress tolerance (Xiao et al., 2015). This wild rice (O. rufipogon Griff.) is evolutionarily more closer to temperate japonica rice and contains several cold-tolerant loci (Mao et al., 2015). Rice cold tolerance and its relationship with spikelet fertility or sterility were also studied (Mitchell et al., 2016). Andaya and Mackill (2003a) used spikelet fertility to identify cold tolerance QTLs during booting stage in RILs obtained by crossing japonica 3 indica (Andaya and Mackill, 2003a). Similarly, cold responsive QTLs in japonica at booting stage were identified using NILs spikelet fertility as trait value (Xu et al., 2008). F2, BC1F1, and BC2F1 derived from a cross (Reiziq 3 Lijiangheigu) were used to detect cold tolerance QTLs that were linked to spikelet sterility in rice (Ye et al., 2010). Other rice cold tolerance QTLs were detected as cold-induced necrosis tolerance (Andaya and Mackill, 2003b), germination ability (Ji et al., 2009; Yang et al., 2017), and maturity stage root chilling tolerance (Xiao et al., 2014). A cold-tolerant rice line was developed by pyramiding cold tolerance QTL which induces tolerance at booting stage (Endo et al., 2016).

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Variable yield performance of different maize lines due to low-temperature indicates the involvement of genetic factor against the low-temperature tolerance. Cold tolerance of maize was assessed through photosynthesis performance and QTL mapping was performed in RILs that identified eight QTLs (Fracheboud et al., 2002). A major QTL for maize cold tolerance photosynthesis was detected on chromosome six using parameters of chlorophyll fluorescence as the trait value (Fracheboud et al., 2004). Two maize inbred lines elite flint and dent were evaluated for chlorophyll fluorescence parameters as cold response, and conducted GWA mapping, which resulted to the detection of some candidate genes (Strigens et al., 2013). These candidate genes were related to ethylene signaling, brassinolide, and lignin biosynthesis, suggesting the occurrence of complex changes in photosynthesis under temperature variations. Cold tolerance QTLs in maize were also detected for root and shoot traits in F2:4 population (Hund et al., 2004). Genomic regions for early plant vigor in maize under cold stress environment was identified using DHLs (Presterl et al., 2007). An F2:3 population obtained by crossing maize inbred lines EP42 (cold-tolerant) and A661 (cold-susceptible) identified QTLs for CTS (Rodrı´guez et al., 2014). The QTL for early seedling development under cold in maize could be a promising genomic region for MAS. Other cold responsive loci were also detected using RILs derived by crossing sweet corn and field corn (Allam et al., 2016). Genetic basis of cold tolerance in legumes such as soybean, pea (P. sativum L.), faba bean (Vicia faba L.), lentil (Lens esculenta), alfalfa (M. sativa L.), M. truncatula have been explored through genetic and QTL mapping. A locus related to chilling tolerance at reproductive growth in soybean was detected in F2 derived by crossing a RIL with a cultivar “Hayahikari” (Funatsuki et al., 2005). In peas a major frost tolerance QTL shared genomic location with a flowering locus Hr (Lejeune-He´naut et al., 2008). Moreover, the frost tolerance QTL of pea colocalized with the genomic regions for sugar contents, such as RuBisCO and raffinose (Dumont et al., 2009), as well as other phenological and morphological characteristics (Klein et al., 2014). QTLs for frost tolerance in faba bean were detected using RILs (Arbaoui et al., 2008; Ali et al., 2016). Association study on faba bean enabled to identify several promising inbred lines that could be used for crop improvement against frost tolerance (Ali et al., 2016). Linkage analysis and GWAS were successfully conducted in faba bean to identify a novel QTL for frost tolerance (Sallam et al., 2016). Genomic locations of M. truncatula freezing tolerance and relevant traits were detected in RILs (Avia et al., 2013). Multiple QTLs associated with winter injury (Li et al., 2015b) and 35 QTLs associated to winter hardiness were identified in alfalfa(Adhikari et al., 2018). Winter frost also impacts the growth and yield of important cereal crops such as wheat. A major QTL controlling frost tolerance in wheat was detected on chromosome 5B using GWA mapping and the QTL was cross validated (Zhao et al., 2013). Two barley loci on chromosome 5H mapped in DHLs showed relation to low-temperature stress (Francia et al., 2004). Comparative genomics study revealed a member of CBF gene family as a component of winter hardiness in barley (Skinner et al., 2006). A new barley QTL, FR-H3, associated to a low-temperature tolerance was detected using DHLs (Fisk et al., 2013), whereas freezing tolerance QTL in two-rowed and six-rowed barley were detected in F2 population using DArT, SSR, and SNP (Tyrka et al., 2015). Frost tolerance related loci in other grass species such as rye (Secale cereale) (Erath et al., 2017), sorghum (Sorghum bicolor) (Knoll et al., 2008;

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Fiedler et al., 2012), and hexaploid oat (Avena sativa L.) (Tumino et al., 2016) were also identified. Also, the genomic region for cold tolerance in other species, such as tomato (Truco et al., 2000; John Goodstal et al., 2005), Arabidopsis (Alonso-Blanco et al., 2005; Meissner et al., 2013), Douglas-fir [Pseudotsuga menziesii (Mirb.)] (Jermstad et al., 2001), Citrus (Weber et al., 2003), and Salix (Tsarouhas et al., 2004) have been reported. These QTLs and related markers are valuable resources for breeding crops against cold stress using MAS.

38.2.6 Salinity stress Salinity stress compromises growth and development of most of the crop species. Poor quality irrigation water and soil salinization are two major causes for salinity stress (Gupta and Huang, 2014). Genetic factors associated with salt stress have been previously investigated in multiple crops such as rice, soybean, cotton, and barley. Rice QTLs associated with transport of salt component ions, such as Na1 and K1, and their ratio (Na1:K1) in shoots and roots were reported in past studies (Flowers et al., 2000; Bonilla et al., 2002; Koyama et al., 2001; Lin et al., 2004). Koyama et al. (2001) reported potential markers useful for breeding salinity tolerant rice. BILs in rice, obtained from two cultivars, Nipponbare and Kasalath, were used for mapping salt tolerance trait and detected 25 QTLs associated with salt tolerance (Takehisa et al., 2004). Genomic loci related to rice adaptation to salinity environment were reported using F2 and F2:3 rice populations (Bimpong et al., 2014). Salinity stress associated candidate genes at the rice seedling stage were identified using integrated RNA sequencing and QTL mapping (Wang et al., 2017). Salinity stress impacts all stages of plants as the salt stress responsive QTLs were identified for various stages of rice such as seed germination (Wang et al., 2011b), seedling development (Wang et al., 2012), and reproductive stage (Hossain et al., 2015). Interestingly, multiple genes within a rice salt stress related QTL, qSaltol, exhibited dynamic impacts depending on the duration of stress, leaf age, and type (Ul Haq et al., 2010). Rice QTL for salt tolerance were also identified in salt-susceptible IL exhibiting transgressive segregation (Qiu et al., 2015). Genomic locations detected for drought stress overlapped with QTLs detected for salinity stress indicating colocalization of abiotic stress related genes. The drought tolerance QTL in rice at chromosome 8 was found to be effective in tolerating salinity stress as well (Nounjan et al., 2016). Rice genome positions linked to an alkaline stress also impacted salt stress tolerance, which was identified using F2:3 and RIL populations (Li et al., 2017; Liang et al., 2015). Chlorate-resistant candidate genes and QTLs for rice were detected using DH population (Teng et al., 2006). Quan et al. (2018) showed that rice elite cultivars can be successfully improved for salt tolerance with wild rice genes through the breeding population (wild 3 elite cultivar) that led to the discovery of QTLs and candidate genes (Quan et al., 2018). Thus, rice has garnered enormous interest in genetics and genomics mechanisms for the salt tolerance. In barley, loci for salt stress related ion homeostasis were detected using DH population (Xue et al., 2009b; Nguyen et al., 2013), that can be utilized in MAS for developing salt-tolerant barley cultivars. Long et al. (2013) performed AM in diverse 192 spring barley accessions and detected a strong QTL and several significant QTLs for salt tolerance and ion content (Na1, K1) in chromosomes 6H and 4H. Salt tolerance in barley was found to

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be linked with other traits such as biomass and height (Long et al., 2013) and stomatal traits (Liu et al., 2014). A salt-tolerant barley cultivar had bigger stomatal aperture than a sensitive cultivar, where the stomatal trait, such as aperture size, was found to correlate with crop yield under salt stress (Liu et al., 2014). Their findings indicated that barley QTL for stomatal traits can be used as surrogate traits for improving the crop against salinity stress. GWAS performed with more than 200 diverse barley accessions led to the detection of a new sQTL for salt tolerance (Fan et al., 2016). Variations present in a barley RIL population to respond to sodium chloride (NaCl) concentration of 250 350 mM led to the detection of associated genomic loci (Ahmadi-Ochtapeh et al., 2015). Genetic mechanisms of salinity stress tolerance have also been focused in the genus Triticum, which includes wheat and related species. A locus (Nax1) for sodium (Na) exclusion was identified in durum wheat on chromosome 2AL (Lindsay et al., 2004), whereas five other markers associated with GY under saline condition were also recorded as potential markers for breeding program (Dura et al., 2013). Other salt tolerance QTLs in T. turgidum were detected on chromosome 4B as revealed by association analysis using SSR markers (Dura et al., 2013). QTLs for Na exclusion and salt stress tolerance were reported for bread wheat (Genc et al., 2010). Forty-five other QTLs related to salt tolerance of wheat during germination and seedling stage were also identified using RILs (Ma et al., 2007). Genomic locations related to salt stress and the interaction of those locations with treatments were reported for T. aestivum (Dı´az De Leo´n et al., 2011; Xu et al., 2012, 2013). Further, QTL analysis conducted for salt tolerance in soybean using F2:5 lines enabled to identify a major QTL flanked by marker Sat_091SSR on LG “N,” which accounted for a genetic variation of B40% 79% in diverse environments (Lee et al., 2004). Some new and previously detected QTL for salt stress were marked on soybean LG “N” (Chen et al., 2008) in a RIL population after field and greenhouse experiments. Genomic location for alkaline salt tolerance (AST) in wild soybean was detected using RIL and F2, where the QTL for AST resided in a different location than QTL for NaCl tolerance is reported earlier (Tuyen et al., 2010). Residual heterozygous lines isolated from RILs were used to validate QTL detection, and high-resolution mapping was also constructed (Tuyen et al., 2013). In another experiment, salt tolerance QTL detected in soybean using RILs was validated by developing salt tolerance NILs (Hamwieh et al., 2011). Therefore the NILs could be a valuable population type to validate the identified QTL in plants. A QTL for salt tolerance that was conserved in wild and cultivated soybean on chromosome 3 was detected using RILs (Ha et al., 2013), whereas a dominant salt tolerance gene was also genetically mapped in cultivated soybean using F2:3 and RILs (Guan et al., 2014). Novel QTL for salinity tolerance in soybean were explored using linkage and AM (Kan et al., 2016). Salt stress related QTLs were identified in several other important horticultural crops. Tomato (Solanum lycopersicum) genomic locations attributing variability in plant salt stress response were explored in two RIL populations obtained from a common female progenitor (Villalta et al., 2007, 2008). The sQTLs associated with amounts of Na1 and K1 in shoot part of the tomato were detected on chromosome seven. Genetic variation present for salt tolerance in Lycopersicon pennellii IL was evidenced by uncovering the presence of many QTLs in saline and nonsaline conditions (Frary et al., 2011). Salt stress impacted cotton growth, lint yield, and fiber quality. QTLs, for salt stress in cotton, were detected using F2:3 interspecific population derived from a cross, Gossypium tomentosum 3 Gossypium hirsutum

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(Oluoch et al., 2016). The study forwarded Gossypium tomentosum, a wild cotton, as a valuable genetic resource for developing salt-tolerant cotton. Abdelraheem et al. (2017) detected several QTLs for salt tolerance in RIL, where the QTLs were present in most of the cotton chromosomes. Salt stress also impacts the growth and yield of chickpea (C. arietinum L.). Two QTLs for chickpea seed yield and number under saline-stress were detected (Vadez et al., 2012). An F2 population of beach cowpea (Vigna luteola 3 Vigna marina subsp. oblonga) harbored one major QTL for salt stress tolerance in V. marina subsp. oblonga (Chankaew et al., 2014). Salt stress related QTLs were also identified in lettuce (L. sativa) (Wei et al., 2014), lotus (Lotus japonicus) (Quero et al., 2014), clover (Trifolium repens L.) (Wang et al., 2010), M. truncatula (Exbrayat et al., 2014), and Arabidopsis (Quesada et al., 2002). This indicates that QTL and candidate gene identification and subsequent MAS could be an appealing approach to improve a vast array of plants against salinity stress.

38.2.7 Flooding/waterlogging/submergence tolerance Waterlogging is another important limiting factor in crop yield potential. Waterlogging is caused by inadequate drainage of soils after rainfall/irrigation or from a rising water level (Reyna et al., 2003). Under water submergence prevents gaseous exchange between soil and atmosphere leading to decrease in oxygen supply (Mommer and Visser, 2005). Decreased oxygen supply further leads to the reduction in crop yield. Studies on submergence tolerance have revealed complex inheritance of the trait. Because of its polygenic nature, breeding for waterlogging tolerance is difficult. It is also challenging to screen many genotypes in field condition. However, measurement of other traits such as aerenchyma formation in roots can be utilized for our convenience. Aerenchyma increases porosity and reduces the resistance during gas transport (Broughton et al., 2015). As a result, aerenchyma formation allows more oxygen to be stored in root tissues. Various studies have been carried out already to detect QTLs associated with aerenchyma formation. Single major QTL for aerenchyma formation after waterlogging treatment was reported in barley DH population (Zhang et al., 2016c). Likewise, three QTLs for aerenchyma formation were identified in wild barley (Zhang et al., 2017). Four QTLs were detected for waterlogging tolerance in barley (Zhou et al., 2012). Similarly, DH population of barley was screened for adventitious root porosity and a single QTL was identified for root porosity as an indicator of aerenchyma formation (Broughton et al., 2015). Eleven QTLs related to waterlogging tolerance in seedling stage were identified in B. napus DH population (Li et al., 2014b). Likewise, 45 QTLs related to waterlogging tolerance were reported in Chrysanthemum (Su et al., 2016). Researchers found two QTLs related to flooding tolerance in Echinochloa (Fukao et al., 2004). Likewise, a study identified 37 QTLs in Lolium for waterlogging tolerance (Pearson et al., 2011). Four QTLs associated with aerenchyma formation in nonflooding conditions were identified in maize (Mano et al., 2007). Twenty-five and thirty-four QTLs for waterlogging condition at seedling stage in maize were identified in the years 2004 and 2005, respectively (Qiu et al., 2007). Five QTLs related to waterlogging tolerance were revealed in Quercus (Parelle et al., 2007) Various researchers have carried out QTL analysis for submergence tolerance in rice. Five QTLs associated with submergence tolerance were identified in rice (Angaji et al., 2010).

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Eleven QTLs associated with LTG and two QTLs for anoxia germinability were found using an F2 rice population (Jiang et al., 2006; Sripongpangkul et al., 2000). Single QTL associated with submergence tolerance was identified by several researchers (Nandi et al., 1997; Xu et al., 2000a,b; Siangliw et al., 2003). Studies conducted by Manangkil et al. (2013), Septiningsih et al. (2012), and Gonzaga et al. (2016) found 32, 4, and 5 QTLs, respectively. In a wheat 3 spelt population, five QTLs related to flooding tolerance were detected (St Burgos et al., 2001). Root development has also been used as an indicator of hypoxia tolerance. In soybean, 11 QTLs for root traits such as length, development, surface area, diameter, and change in average root diameter were identified; 7 QTLs were identified for hypoxia tolerance of these root traits (Van Nguyen et al., 2017). Adventitious root formation (ARF) is another form of adaptation to waterlogging in plants, and five QTLs were detected in teosinte for ARF (Yoshiro et al., 2005).

38.2.8 Stay-green attribute Stay-green (also known as delayed senescence) is a term to describe delayed foliar senescence in plant species. It is regarded as a key indicator of abiotic stress tolerance in crops (Lopes and Reynolds, 2012; Thomas and Ougham, 2014). Although it had been established as a superior trait in the 1970s, it only gained wide attention in the early 20th century, after which it has been utilized as a selection criterion for abiotic stress tolerance (Thomas and Ougham, 2014). Plant breeders have been studying the genetic architecture of the staygreen trait in various crops such as sorghum (Tuinstra et al., 1997; Xu et al., 2000a,b; Sanchez et al., 2002; Harris, 2007), rice (Cha et al., 2002; Fu et al., 2011), maize (Zheng et al., 2009; Wang et al., 2012), barley (Gous et al., 2016), and wheat (Kumar et al., 2010). Genetic variability for stay-green trait has been identified and exploited in many crops including rice, wheat, maize, fescue, oat, soybean, tomato, pea, pepper, and other species (Armstead et al., 2006; Barry et al., 2008; Thomas and Smart, 1993; Duvick et al., 2004; Thomas and Stoddart, 1975). In sorghum, stay-green QTLs have been reported in drought conditions (Awika et al., 2017; Kebede et al., 2001; Tao et al., 2000) as well as optimum environmental conditions (Harris et al., 2006; Sanchez et al., 2002; Xu et al., 2000a,b). Xu et al. (2000a,b) identified four stay-green QTLs in RILs in three LGs. Stg1 and Stg2 QTLs on LG A explained 13% 20% and 20% 30% of the phenotypic variance, respectively. Stg3 and Stg4 QTLs were identified on LGs D and J. Similarly, Harris (2007) reported four QTLs related to stay-green trait in sorghum. Pinto et al. (2016) reported QTLs for stay-green trait in wheat under heat stress. They identified QTLs on 2A, 4B, 4D, 6A, and 7D chromosomes. A locus on chromosome 7D accounted for 15% of the variance. Furthermore, Christopher et al. (2018) identified QTL regions related to stay-green in both dry and wet environments, on chromosomes 4A, 4B, 4D.

38.3 Concluding remarks and future perspectives Agricultural practices are ever evolving, and target environments are also changing. Crop needs to adapt accordingly to changing farming practices and environments. Rising

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population, increasing pollution, and emerging insect pathogen races challenge plant breeder and scientists. Selection of plants with desirable traits for increased yield, biotic and abiotic stress is a primary focus of plant breeders. Crop loss due to biotic and abiotic stress can be minimized by developing stress-tolerant cultivars through manipulation of associated genes and genomic regions. The identification of QTLs associated with stresses should help plant breeders to develop stress-resistant varieties of important crops. Considering the present and future problems of plant mineral nutrition, identification and development of mineral-efficient genotypes that are less dependent on the heavy application of fertilizers would be a sustainable and economical approach. Quantitative traits are affected by environmental factors and gene interactions. QTL study performed in one environment only likely underestimate the number of QTLs for a trait. Therefore, QTL analysis done on multiple environments increases the reliability and consistency of QTL detected. Success of QTL mapping lies in the selection of parents and traits. The parents that are selected to develop a mapping population should differ from the traits of interest. QTLs will be detected for those traits that are contrasting in parents and segregates in progeny (Koide et al., 2013; Qiu et al., 2014). Studies on QTL identification will become useful when identified QTLs introgressed into an elite background of relevant crops. The conserved regions conferring adaptation across grass species can be applied for improving tolerance in cereals. Although several reports published elsewhere in the literature indicates QTLs identified for economically important traits, few of them introgressed into elite genotypes (Abe, 1989; Endo et al., 2016). Over the last few years, mapping of QTLs for economically important traits and genome assembly has largely facilitated the breeding programs by the development of MAS (Wang et al., 2011c). Majority of QTLs detected in many studies are environment specific. Precise estimation and validation limit the application of these QTLs in a breeding program. QTLs that are expressed over experiment, year, and condition for more traits, that is, sQTL clusters, are suitable for MAS. Choice of parents in QTL mapping is a critical step. Although parents are contrasting for a trait, both parents can harbor high-value alleles. Choice of mapping population is also equally important, where segregating populations such as F2, F3, BC are faster to develop. However, RIL and DH can be maintained and produced for eternity and allows replicated and repeated experiments. Once precise QTLs get identified, fine mapping needs to be done in order to narrow down the QTL to candidate genes. Combining multiple trait-multiple QTLs is always a successful strategy than relying on single trait single QTL. Progress has been made in improving stress tolerance by using QTLs. However, an integrated strategy combining interdisciplinary approaches, such as crop modeling, phenomics, genetics, and genomics, would be more efficient to improve stress tolerance in crops (Varshney et al., 2018b). After a QTL is identified, next steps are to deploy them into MAS, fine mapping, candidate gene identification, and cloning of the gene underlying the QTL. QTLs identified from analysis should be validated since the distance between linked QTLs, magnitude of effects of individual QTLs, environmental effects, mapping population size, and experimental errors influence accuracy of QTLs. QTL studies replicated across sites and over time allow to study environmental effects on QTL. Increasing the population size allows precise R2 estimation and detection of most QTLs and QTLs with small effects. Due to the factors above described, QTL position and effects should be independently verified using same parental genotypes

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References

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or closely related genotypes or in independent populations. After a reliable and tightly linked markers with the phenotype is identified, it may be used for MAS. QTL identification has enabled us to link variations at the trait level to those at the sequence level. Since a QTL can harbor tens to hundreds of genes (Gelli et al., 2016), the identification of genes responsible for phenotypic variation poses a major challenge. Accurate identification of the underlying genes responsible for trait variation in QTL regions is difficult in many crops due to the lack of genomic and transcriptomic resources. Nevertheless, the comparative genomic approach utilizing reference genome of the close relative has helped us to identify putative candidate genes related to abiotic stresses in plants. Conventional breeding approaches have been traditionally used to develop stresstolerant crop plants by harnessing variability existing in the germplasm collection. However, biotechnological tools are continuously explored to complement conventional breeding approaches. Plants growing under natural condition must cope with several abiotic stresses to ensure their better survival. Improving crops against abiotic stress requires proper understanding of the genetic basis of the traits which could be achieved by linkage, QTL, and AM. Markers and QTLs identified in a specific population and verified using broad population are valuable resources that can be used in breeding programs for MAS. QTLs that are expressed regardless of the environmental interactions would be a valuable source for transferring the genes/QTLs to elite lines and releasing new cultivars with enhanced trait values.

References Abe, N., 1989. Development of the “Rice Norin-PL8” with high tolerance to cool temperature at the booting stage. Res. Bull. Hokkaido. Agric. Exp. Stn. 152, 9 17. Abdel-Haleem, H., Carter, T.E., Rufty, T.W., Boerma, H.R., Li, Z., 2014. Quantitative trait loci controlling aluminum tolerance in soybean: candidate gene and single nucleotide polymorphism marker discovery. Mol. Breed. 33 (4), 851 862. Available from: https://doi.org/10.1007/s11032-013-9999-5. Abdelraheem, A., Mahdy, E., Zhang, J., 2015. The first linkage map for a recombinant inbred line population in cotton (Gossypium barbadense) and its use in studies of PEG-induced dehydration tolerance. Euphytica 205 (3), 941 958. Abdelraheem, A., Fang, D.D., Zhang, J., 2017. Quantitative trait locus mapping of drought and salt tolerance in an introgressed recombinant inbred line population of upland cotton under the greenhouse and field conditions. Euphytica 214, 8. Adhikari, L., Missaoui, A.M., 2017. Nodulation response to molybdenum supplementation in alfalfa and its correlation with root and shoot growth in low pH soil. J. Plant Nutr. 40 (16), 2290 2302. Adhikari, L., Lindstrom, O.M., Markham, J., Missaoui, A.M., 2018. Dissecting key adaptation traits in the polyploid perennial Medicago sativa using GBS-SNP mapping. Front. Microbiol. 9, 1 19. Available from: https:// doi.org/10.3389/fpls.2018.00934. Ahmadi-Ochtapeh, H., Soltanloo, H., Ramezanpour, S., Naghavi, M., Nikkhah, H., Rad, S.Y., 2015. QTL mapping for salt tolerance in barley at seedling growth stage. Biol. Plant. 59, 283 290. Aimar, D., Calafat, M., Andrade, A.M., Carassay, L., Abdala, G.I., Molas, M.L., 2011. Drought tolerance and stress hormones: from model organisms to forage crops. Plants Environ. 137 164. Available from: https://doi.org/ 10.5772/1958 (April 2014). Ali, M.L., Pathan, M.S., Zhang, J., Bai, G., Sarkarung, S., Nguyen, H.T., 2000. Mapping QTLs for root traits in a recombinant inbred population from two indica ecotypes in rice. TAG Theor. Appl. Genet. 101 (5 6), 756 766. Available from: https://doi.org/10.1007/s001220051541.

Plant Life under Changing Environment

946

38. Use of quantitative trait loci to develop stress tolerance in plants

Ali, M.B., Ibrahim, A.M.H., Malla, S., Rudd, J., Hays, D.B., 2013. Family-based QTL mapping of heat stress tolerance in primitive tetraploid wheat (Triticum turgidum L.). Euphytica 192, 189 203. Ali, M.B.M., Welna, G.C., Sallam, A., Martsch, R., Balko, C., Gebser, B., et al., 2016. Association analyses to genetically improve drought and freezing tolerance of faba bean (Vicia faba L.). Crop Sci. 56, 1036 1048. Allam, M., Revilla, P., Djemel, A., Tracy, W.F., Orda´s, B., 2016. Identification of QTLs involved in cold tolerance in sweet 3 field corn. Euphytica 208, 353 365. Alonso-Blanco, C., Gomez-Mena, C., Llorente, F., Koornneef, M., Salinas, J., Martı´nez-Zapater, J.M., 2005. Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol. 139, 1304 1312. Andaya, V., Mackill, D., 2003a. QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica 3 indica cross. TAG Theor. Appl. Genet. 106, 1084 1090. Andaya, V.C., Mackill, D.J., 2003b. Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J. Exp. Bot. 54, 2579 2585. Andaya, V.C., Tai, T.H., 2006. Fine mapping of the qcts12 locus, a major QTL for seedling cold tolerance in rice. TAG Theor. Appl. Genet. 113, 467 475. Anderson, J., 1993. Selenium interactions in sulfur metabolism. In: De Kok, L. (Ed.), Sulfur Nutrition and Assimilation in Higher Plants Regulatory, Agricultural and Environmental Aspects. SPB Academic Publishing, The Hague, The Netherlands, pp. 49 60. Angaji, S.A., Septiningsih, E.M., Mackill, D.J., Ismail, A.M., 2010. QTLs associated with tolerance of flooding during germination in rice (Oryza sativa L.). Euphytica 172 (2), 159 168. Available from: https://doi.org/10.1007/ s10681-009-0014-5. Aparna, K., Nepolean, T., Srivastsava, R.K., Kholova´, J., Rajaram, V., Kumar, S., et al., 2015. Quantitative trait loci associated with constitutive traits control water use in pearl millet [Pennisetum glaucum (L.) R. Br.]. Plant Biol. 17 (5), 1073 1084. Arbaoui, M., Link, W., Satovic, Z., Torres, A.-M., 2008. Quantitative trait loci of frost tolerance and physiologically related trait in faba bean (Vicia faba L.). Euphytica 164, 93 104. Arcade, A., Labourdette, A., Falque, M., Mangin, B., Chardon, F., Charcosset, A., et al., 2004. BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20 (14), 2324 2326. Available from: https://doi.org/10.1093/bioinformatics/bth230. Armstead, I., Donnison, I., Aubry, S., Harper, J., Ho¨rtensteiner, S., James, C., et al., 2006. From crop to model to crop: identifying the genetic basis of the staygreen mutation in the Lolium/Festuca forage and amenity grasses. New Phytol. 172, 592 597. Asfaw, A., Blair, M.W., 2012. Quantitative trait loci for rooting pattern traits of common beans grown under drought stress versus non-stress conditions. Mol. Breed. 30 (2), 681 695. Avia, K., Pilet-Nayel, M.-L., Bahrman, N., Baranger, A., Delbreil, B., Fontaine, V., et al., 2013. Genetic variability and QTL mapping of freezing tolerance and related traits in Medicago truncatula. TAG Theor. Appl. Genet. 126, 2353 2366. Awika, H.O., Hays, D.B., Mullet, J.E., Rooney, W.L., Weers, B.D., 2017. QTL mapping and loci dissection for leaf epicuticular wax load and canopy temperature depression and their association with QTL for staygreen in Sorghum bicolor under stress. Euphytica 213 (9), 207. Awlachew, Z.T., Singh, R., Kaur, S., Bains, N.S., Chhuneja, P., 2016. Transfer and mapping of the heat tolerance component traits of Aegilops speltoides in tetraploid wheat Triticum durum. Mol. Breed. 36, 78. Azam, F.I., Chang, X., Jing, R., 2015. Mapping QTL for chlorophyll fluorescence kinetics parameters at seedling stage as indicators of heat tolerance in wheat. Euphytica 202, 245 258. Bajji, M., Kinet, J.M., Lutts, S., 2002. The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul. 36 (1), 61 70. Baligar, V.C., Fageria, N.K., He, Z.L., 2001. Nutrient use efficiency in plants. Commun. Soil Sci. Plant Anal. 32 (7 8), 921 950. Ba´lint, A.F., Ro¨der, M.S., Hell, R., Galiba, G., Bo¨rner, A., 2007. Mapping of QTLs affecting copper tolerance and the Cu, Fe, Mn and Zn contents in the shoots of wheat seedlings. Biol. Plant. 51 (1), 129 134. Available from: https://doi.org/10.1007/s10535-007-0025-9. Barry, C.S., McQuinn, R.P., Chung, M.-Y., Besuden, A., Giovannoni, J.J., 2008. Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol. 147, 179 187.

Plant Life under Changing Environment

References

947

Basto, S., Thompson, K., Grime, J.P., Fridley, J.D., Calhim, S., Askew, A.P., et al., 2018. Severe effects of long-term drought on calcareous grassland seed banks. npj Clim. Atmos. Sci. 1 (1), 1. Becquer, T., Quantin, C., Sicot, M., Boudot, J.P., 2003. Chromium availability in ultramafic soils from New Caledonia. Sci. Total Environ. 301 (1 3), 251 261. Available from: https://doi.org/10.1016/S0048-9697(02) 00298-X. Beebe, S.E., Rojas-Pierce, M., Yan, X., Blair, M.W., Pedraza, F., Mun˜oz, F., et al., 2006. Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci. 46 (1), 413. Available from: https://doi.org/10.2135/cropsci2005.0226. Beecher, F.W., Mason, E., Mondal, S., Awika, J., Hays, D., Ibrahim, A., 2012. Identification of quantitative trait loci (QTLs) associated with maintenance of wheat (Triticum aestivum Desf.) quality characteristics under heat stress conditions. Euphytica 188, 361 368. Bert, P.-F., Bordenave, L., Donnart, M., He´vin, C., Ollat, N., Decroocq, S., 2013. Mapping genetic loci for tolerance to lime-induced iron deficiency chlorosis in grapevine rootstocks (Vitis sp.). TAG Theor. Appl. Genet. 126 (2), 451 473. Available from: https://doi.org/10.1007/s00122-012-1993-5. Bertioli, D.J., et al., 2016. The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut. Nat. Genet. 48, 438 446. Bianchi-Hall, C.M., Carter, T.E., Bailey, M.A., Mian, M.A.R., Rufty, T.W., Ashley, D.A., et al., 2000. Aluminum tolerance associated with quantitative trait loci derived from soybean PI 416937 in hydroponics. Crop Sci. Available from: https://doi.org/10.2135/cropsci2000.402538x. Bimpong, I.K., Manneh, B., Diop, B., Ghislain, K., Sow, A., Amoah, N.K.A., et al., 2014. New quantitative trait loci for enhancing adaptation to salinity in rice from Hasawi, a Saudi landrace into three African cultivars at the reproductive stage. Euphytica 200, 45 60. Boardman, N.K., 1975. Trace Elements in Photosynthesis, vol. 199. Academic Press, New York. Bode, K., Doring, O., Luthje, S., Neue, H.-U., Bottger, M., 1995. The role of active oxygen in iron tolerance of rice (Oryza sativa L.). Protoplasm 184, 249 255. Available from: https://doi.org/10.1007/BF012.76928. Bonilla, P., Dvorak, J., Mackell, D., Deal, K., Gregorio, G., 2002. RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philipp. Agric. Sci. (Philippines) 65, 68 76. Branham, S.E., Stansell, Z.J., Couillard, D.M., Farnham, M.W., 2017. Quantitative trait loci mapping of heat tolerance in broccoli (Brassica oleracea var. Italica) using genotyping-by-sequencing. TAG Theor. Appl. Genet. 130, 529 538. Broughton, S., Zhou, G., Teakle, N.L., Matsuda, R., Zhou, M., O’Leary, R.A., et al., 2015. Waterlogging tolerance is associated with root porosity in barley (Hordeum vulgare L.). Mol. Breed. 35 (1). Available from: https://doi. org/10.1007/s11032-015-0243-3. Burton, A.L., Johnson, J.M., Foerster, J.M., Hirsch, C.N., Buell, C.R., Hanlon, M.T., et al., 2014. QTL mapping and phenotypic variation for root architectural traits in maize (Zea mays L.). TAG Theor. Appl. Genet. 127 (11), 2293 2311. Cai, S., Bai, G.-H., Zhang, D., 2008. Quantitative trait loci for aluminum tolerance in Chinese wheat landrace FSW. Theor. Appl. Genet. 117, 49 56. Available from: https://doi.org/10.1007/s10681-012-0807-9. Caires, E., Garbuio, F., Churka, S., Barth, G., Correa, J., 2008. Effects of soil acidity amelioration by surface liming on no-till corn, soybean, and wheat root growth and yield. Eur. J. Agron. 28 (1), 57 64. Available from: https://doi.org/10.1016/j.eja.2007.05.002. Cartwright, B., Zarcinas, B., Mayfield, A., 1984. Toxic concentrations of boron in a red-brown early at Gladstone, South Australia. Aust. J. Soil Res. 22, 261 272. Cassan, L., Moreau, L., Segouin, S., Bellamy, A., Falque, M., Limami, A.M., 2010. Genetic map construction and quantitative trait loci (QTL) mapping for nitrogen use efficiency and its relationship with productivity and quality of the biennial crop Belgian endive (Cichorium intybus L.). J. Plant Physiol. 167 (15), 1253 1263. Available from: https://doi.org/10.1016/J.JPLPH.2010.04.016. Cha, K.W., Lee, Y.J., Koh, H.J., Lee, B.M., Nam, Y.W., Paek, N.C., 2002. Isolation, characterization, and mapping of the stay green mutant in rice. TAG Theor. Appl. Genet. 104 (4), 526 532. Champoux, M.C., Wang, G., Sarkarung, S., Mackill, D.J., O’Toole, J.C., Huang, N., et al., 1995. Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers. TAG Theor. Appl. Genet. 90 (7 8), 969 981. Available from: https://doi.org/10.1007/BF00222910.

Plant Life under Changing Environment

948

38. Use of quantitative trait loci to develop stress tolerance in plants

Chankaew, S., Isemura, T., Naito, K., Ogiso-Tanaka, E., Tomooka, N., Somta, P., et al., 2014. QTL mapping for salt tolerance and domestication-related traits in Vigna marina subsp. oblonga, a halophytic species. TAG Theor. Appl. Genet. 127, 691 702. Chen, H., Cui, S., Fu, S., Gai, J., Yu, D., 2008. Identification of quantitative trait loci associated with salt tolerance during seedling growth in soybean (Glycine max L.). Aust. J. Agric. Res. 59, 1086 1091. Chen, J., Xu, L., Cai, Y., Xu, J., 2009. Identification of QTLs for phosphorus utilization efficiency in maize (Zea mays L.) across P levels. Euphytica 167 (2), 245 252. Available from: https://doi.org/10.1007/s10681-009-9883-x. Chen, J., Chang, S.X., Anyia, A.O., 2012. Quantitative trait loci for water-use efficiency in barley (Hordeum vulgare L.) measured by carbon isotope discrimination under rain-fed conditions on the Canadian Prairies. TAG Theor. Appl. Genet. 125 (1), 71 90. Available from: https://doi.org/10.1007/s00122-012-1817-7. Christopher, M., Chenu, K., Jennings, R., Fletcher, S., Butler, D., Borrell, A., et al., 2018. QTL for stay-green traits in wheat in well-watered and water-limited environments. Field Crops Res. 217, 32 44. Clark, R.B., 1982. Plant response to mineral element toxicity and deficiency. In: Christiansen, M.N., Lewis, C.F. (Eds.), Breeding Plants for Less Favorable Environments. John Wiley & Sons, New York, pp. 71 142. Cui, K., Huang, J., Xing, Y., Yu, S., Xu, C., Peng, S., 2008. Mapping QTLs for seedling characteristics under different water supply conditions in rice (Oryza sativa). Physiol. Plant. 132 (1), 53 68. Available from: https://doi. org/10.1111/j.1399-3054.2007.00991.x. Cui, L., Shan, J., Shi, M., Gao, J., Lin, H., 2014. The miR156-SPL 9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J. 80, 1108 1117. Cui, F., Fan, X., Chen, M., Zhang, N., Zhao, C., Zhang, W., et al., 2016. QTL detection for wheat kernel size and quality and the response of these traits to low nitrogen stress. TAG Theor. Appl. Genet. 129 (3), 469 484. Dai, J., Bai, G., Zhang, D., Hong, D., 2013. Validation of quantitative trait loci for aluminum tolerance in Chinese wheat landrace FSW. Euphytica 192 (2), 171 179. Available from: https://doi.org/10.1007/s10681012-0807-9. Dias, P.M.B., Brunel-Muguet, S., Du¨rr, C., Huguet, T., Demilly, D., Wagner, M.-H., et al., 2011. QTL analysis of seed germination and pre-emergence growth at extreme temperatures in Medicago truncatula. TAG Theor. Appl. Genet. 122, 429 444. Dı´az De Leo´n, J.L., Escoppinichi, R., Geraldo, N., Castellanos, T., Mujeeb-Kazi, A., Ro¨der, M.S., 2011. Quantitative trait loci associated with salinity tolerance in field grown bread wheat. Euphytica 181, 371 383. Ding, G., Zhao, Z., Liao, Y., Hu, Y., Shi, L., Long, Y., et al., 2012. Quantitative trait loci for seed yield and yieldrelated traits, and their responses to reduced phosphorus supply in Brassica napus. Ann. Bot. 109 (4), 747 759. Available from: https://doi.org/10.1093/aob/mcr323. Dixit, V., Pandey, V., Shyam, R., 2002. Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria. Plant Cell Environ. 25 (5), 687 693. Available from: https://doi.org/10.1046/j.1365-3040.2002.00843.x. Doerge, R.W., 2002. Multifactorial genetics: mapping and analysis of quantitative trait loci in experimental populations. Nat. Rev. Genet. 3 (1), 43 52. Available from: https://doi.org/10.1038/nrg703. Dong, Y., Ogawa, T., Lin, D., Koh, H.J., Kamiunten, H., Matsuo, M., et al., 2006. Molecular mapping of quantitative trait loci for zinc toxicity tolerance in rice seedling (Oryza sativa L.). Field Crops Res. 95 (2 3), 420 425. Available from: https://doi.org/10.1016/j.fcr.2005.03.005. Dufey, I., Hakizimana, P., Draye, X., Lutts, S., Bertin, P., 2009. QTL mapping for biomass and physiological parameters linked to resistance mechanisms to ferrous iron toxicity in rice. Euphytica 167 (2), 143 160. Available from: https://doi.org/10.1007/s10681-008-9870-7. Dufey, I., Hiel, M.P., Hakizimana, P., Draye, X., Lutts, S., Kone´, B., et al., 2012. Multienvironment quantitative trait loci mapping and consistency across environments of resistance mechanisms to ferrous iron toxicity in rice. Crop Sci. 52 (2), 539 550. Available from: https://doi.org/10.2135/cropsci2009.09.0544. Dufey, I., Draye, X., Lutts, S., Lorieux, M., Martinez, C., Bertin, P., 2015. Novel QTLs in an interspecific backcross Oryza sativa 3 Oryza glaberrima for resistance to iron toxicity in rice. Euphytica 204 (3), 609 625. Available from: https://doi.org/10.1007/s10681-014-1342-7. Dumont, E., Fontaine, V., Vuylsteker, C., Sellier, H., Bode`le, S., Voedts, N., et al., 2009. Association of sugar content QTL and PQL with physiological traits relevant to frost damage resistance in pea under field and controlled conditions. TAG Theor. Appl. Genet. 118, 1561 1571.

Plant Life under Changing Environment

References

949

Dura, S., Duwayri, M., Nachit, M., Al Sheyab, F., 2013. Detection of molecular markers associated with yield and yield components in durum wheat (Triticum turgidum L. var. durum) under saline conditions. Crop Pasture Sci. 64, 957 964. Duvick, D.N., Smith, J.S.C., Cooper, M., 2004. Long-term selection in a commercial hybrid maize breeding program. Plant Breed. Rev. 24, 109 152. Elliott, J., Glotter, M., Ruane, A.C., Boote, K.J., Hatfield, J.L., Jones, J.W., et al., 2018. Characterizing agricultural impacts of recent large-scale US droughts and changing technology and management. Agric. Syst. 159, 275 281. Endo, T., Chiba, B., Wagatsuma, K., Saeki, K., Ando, T., Shomura, A., et al., 2016. Detection of QTLs for cold tolerance of rice cultivar ‘Kuchum’ and effect of QTL pyramiding. TAG Theor. Appl. Genet. 129, 631 640. Epstein, E., 1961. Mineral metabolism of halophytes. In: Rorison, I.H. (Ed.), Ecological Aspects of the Mineral Nutrition of Plants. Blackwell Publishers, Oxford, Edinburg, UK, pp. 345 353. Epstein, E., Hagen, C.E., 1952. A kinetic study of the absorption of alkali cations by barley roots. Plant Physiol. 27, 457 474. Erath, W., Bauer, E., Fowler, D.B., Gordillo, A., Korzun, V., Ponomareva, M., et al., 2017. Exploring new alleles for frost tolerance in winter rye. TAG Theor. Appl. Genet. 130, 2151 2164. Esten Mason, R., Mondal, S., Beecher, F.W., Hays, D.B., 2011. Genetic loci linking improved heat tolerance in wheat (Triticum aestivum L.) to lower leaf and spike temperatures under controlled conditions. Euphytica 180, 181 194. Exbrayat, S., Bertoni, G., Naghavie, M.R., Peyghambari, A., Badri, M., Debelle, F., 2014. Genetic variability and identification of quantitative trait loci affecting plant growth and chlorophyll fluorescence parameters in the model legume Medicago truncatula under control and salt stress conditions. Funct. Plant Biol. 41, 983 1001. Fan, Y., Zhou, G., Shabala, S., Chen, Z.-H., Cai, S., Li, C., et al., 2016. Genome-wide association study reveals a new QTL for salinity tolerance in barley (Hordeum vulgare L.). Front. Plant Sci. 7, 946. Faye, I., Pandey, M.K., Hamidou, F., Rathore, A., Ndoye, O., Vadez, V., et al., 2015. Identification of quantitative trait loci for yield and yield related traits in groundnut (Arachis hypogaea L.) under different water regimes in Niger and Senegal. Euphytica 206 (3), 631 647. Available from: https://doi.org/10.1007/s10681015-1472-6. Feng, Y., Cao, L.Y., Wu, W.M., Shen, X.H., Zhan, X.D., Zhai, R.R., et al., 2010. Mapping QTLs for nitrogendeficiency tolerance at seedling stage in rice (Oryza sativa L.). Plant Breed. 129 (6), 652 656. Available from: https://doi.org/10.1111/j.1439-0523.2009.01728.x. Fiedler, K., Bekele, W.A., Friedt, W., Snowdon, R., Stu¨tzel, H., Zacharias, A., et al., 2012. Genetic dissection of the temperature dependent emergence processes in sorghum using a cumulative emergence model and stability parameters. TAG Theor. Appl. Genet. 125, 1647 1661. Fisk, S.P., Cuesta-Marcos, A., Cistue´, L., Russell, J., Smith, K.P., Baenziger, S., et al., 2013. FR-H3: a new QTL to assist in the development of fall-sown barley with superior low temperature tolerance. TAG Theor. Appl. Genet. 126, 335 347. Flowers, T., Koyama, M., Flowers, S., Sudhakar, C., Singh, K., Yeo, A., 2000. QTL: Their place in engineering tolerance of rice to salinity. J. Exp. Bot. 51, 99 106. Fracheboud, Y., Ribaut, J.M., Vargas, M., Messmer, R., Stamp, P., 2002. Identification of quantitative trait loci for cold-tolerance of photosynthesis in maize (Zea mays L.). J. Exp. Bot. 53, 1967 1977. Fracheboud, Y., Jompuk, C., Ribaut, J.M., Stamp, P., Leipner, J., 2004. Genetic analysis of cold-tolerance of photosynthesis in maize. Plant Mol. Biol. 56, 241 253. Francia, E., Rizza, F., Cattivelli, L., Stanca, A.M., Galiba, G., To´th, B., et al., 2004. Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) 3 ‘Tremois’ (spring) barley map. TAG Theor. Appl. Genet. 108, 670 680. ˘ Frary, A., Kele¸s, D., Pinar, H., Go¨l, D., Doganlar, S., 2011. NaCl tolerance in Lycopersicon pennellii introgression lines: QTL related to physiological responses. Biol. Plant. 55, 461 468. Fu, J.-D., Yan, Y.-F., Kim, M.Y., Lee, S.-H., Lee, B.-W., 2011. Population-specific quantitative trait loci mapping for functional stay-green trait in rice (Oryza sativa L.). Genome 54, 235 243. Fukao, T., Paterson, A.H., Hussey, M.A., Yamasue, Y., Kennedy, R.A., Rumpho, M.E., 2004. Construction of a comparative RFLP map of Echinochloa crus-galli toward QTL analysis of flooding tolerance. TAG Theor. Appl. Genet. 108 (6), 993 1001. Available from: https://doi.org/10.1007/s00122-003-1530-7.

Plant Life under Changing Environment

950

38. Use of quantitative trait loci to develop stress tolerance in plants

Funatsuki, H., Kawaguchi, K., Matsuba, S., Sato, Y., Ishimoto, M., 2005. Mapping of QTL associated with chilling tolerance during reproductive growth in soybean. TAG Theor. Appl. Genet. 111, 851 861. Gallais, A., 1984. An analysis of heterosis vs. inbreeding effects with an autotetraploid cross-fertilized plant: Medicago sativa L. Genetics 106, 123 137. Garbisu, C., Alkorta, I., 2003. Basic concepts on heavy metal soil bioremediation. Eur. J. Miner. Process. Environ. Prot. 3, 58 66. Geisseler, D., Miyao, G., 2016. Soil testing for P and K has value in nutrient management for annual crops. Calif. Agric. 70 (3), 152 159. Gelli, M., Mitchell, S.E., Liu, K., Clemente, T.E., Weeks, D.P., Zhang, C., et al., 2016. Mapping QTLs and association of differentially expressed gene transcripts for multiple agronomic traits under different nitrogen levels in sorghum. BMC Plant Biol. 16 (16), 1 18. Available from: https://doi.org/10.1186/s12870-015-0696-x. Gemenet, D.C., Leiser, W.L., Zangre, R.G., Angarawai, I.I., Sanogo, M.D., Sy, O., et al., 2015. Association analysis of low-phosphorus tolerance in West African pearl millet using DArT markers. Mol. Breed. 35 (8), 171. Available from: https://doi.org/10.1007/s11032-015-0361-y. Genc, Y., Oldach, K., Verbyla, A.P., Lott, G., Hassan, M., Tester, M., et al., 2010. Sodium exclusion QTL associated with improved seedling growth in bread wheat under salinity stress. TAG Theor. Appl. Genet. 121, 877 894. Gonzaga, Z.J.C., Carandang, J., Sanchez, D.L., Mackill, D.J., Septiningsih, E.M., 2016. Mapping additional QTLs from FR13A to increase submergence tolerance in rice beyond SUB1. Euphytica 209, 627 636. Gous, P.W., Hickey, L., Christopher, J.T., Franckowiak, J., Fox, G.P., 2016. Discovery of QTL for stay-green and heatstress in barley (Hordeum vulgare) grown under simulated abiotic stress conditions. Euphytica 207 (2), 305 317. Gross, J., Stein, R.J., Fett-Neto, A.G., Fett, J.P., 2003. Iron homeostasis related genes in rice. Genet. Mol. Biol. 26 (4), 477 497. Available from: https://doi.org/10.1590/S1415-47572003000400012. Gu, J., Yin, X., Struik, P.C., Stomph, T.J., Wang, H., 2012. Using chromosome introgression lines to map quantitative trait loci for photosynthesis parameters in rice (Oryza sativa L.) leaves under drought and well-watered field conditions. J. Exp. Bot. 63 (1), 455 469. Available from: https://doi.org/10.1093/jxb/ err292. Guan, R., Chen, J., Jiang, J., Liu, G., Liu, Y., Tian, L., et al., 2014. Mapping and validation of a dominant salt tolerance gene in the cultivated soybean (Glycine max) variety Tiefeng 8. Crop J. 2, 358 365. Guo, P., Baum, M., Varshney, R.K., Graner, A., Grando, S., Ceccarelli, S., 2008. QTLs for chlorophyll and chlorophyll fluorescence parameters in barley under post-flowering drought. Euphytica 163 (2), 203 214. Guo, J., Chen, G., Zhang, X., Li, T., Yu, H., Chen, H., 2017. Mapping quantitative trait loci for tolerance to phosphorus-deficiency at the seedling stage in barley. Euphytica 213 (6), 114. Available from: https://doi.org/ 10.1007/s10681-017-1907-3. Gupta, B., Huang, B., 2014. Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int. J. Genomics 2014, 701596. Gutie´rrez, A.A., Engle, N.L., Nys, E.D., Molejo´n, C., Martins, E.S., 2014. Drought preparedness in Brazil. Weather Clim. Extremes 3, 95 106. Available from: https://doi.org/10.1016/j.wace.2013.12.001. Ha, B.-K., Vuong, T.D., Velusamy, V., Nguyen, H.T., Grover Shannon, J., Lee, J.-D., 2013. Genetic mapping of quantitative trait loci conditioning salt tolerance in wild soybean (Glycine soja) PI 483463. Euphytica 193, 79 88. Hamwieh, A., Tuyen, D.D., Cong, H., Benitez, E.R., Takahashi, R., Xu, D.H., 2011. Identification and validation of a major QTL for salt tolerance in soybean. Euphytica 179, 451 459. Hamwieh, A., Imtiaz, M., Malhotra, R.S., 2013. Multi-environment QTL analyses for drought-related traits in a recombinant inbred population of chickpea (Cicer arietinum L.). TAG Theor. Appl. Genet. 126 (4), 1025 1038. Available from: https://doi.org/10.1007/s00122-012-2034-0. Harris, K., Subudhi, P.K., Borrell, A., Jordan, D., Rosenow, D., Nguyen, H., et al., 2006. Sorghum stay-green QTL individually reduce post-flowering drought-induced leaf senescence. J. Exp. Bot. 58 (2), 327 338. Harris, K., 2007. Genetic analysis of the Sorghum bicolor stay-green drought tolerance trait. Doctoral dissertation, Texas A&M University, College Station, TX. Hassan, M., Oldach, K., Baumann, U., Langridge, P., Sutton, T., 2010. Genes mapping to boron tolerance QTL in barley identified by suppression subtractive hybridization. Plant Cell Environ. 33 (2), 188 198. Available from: https://doi.org/10.1111/j.1365-3040.2009.02069.x. Hayes, J.E., Pallotta, M., Baumann, U., Berger, B., Langridge, P., Sutton, T., 2013. Germanium as a tool to dissect boron toxicity effects in barley and wheat. Funct. Plant Biol. 40 (6), 618 627. Available from: https://doi.org/ 10.1071/FP12329.

Plant Life under Changing Environment

References

951

Herve´, D., Fabre, F., Berrios, E.F., Leroux, N., Al Chaarani, G., Planchon, C., et al., 2001. QTL analysis of photosynthesis and water status traits in sunflower (Helianthus annuus L.) under greenhouse conditions. J. Exp. Bot. 52 (362), 1857 1864. Available from: https://doi.org/10.1093/jexbot/52.362.1857. Hirabayashi, H., Sasaki, K., Kambe, T., Gannaban, R.B., Miras, M.A., Mendioro, M.S., et al., 2015. qEMF3, a novel QTL for the early-morning flowering trait from wild rice, Oryza officinalis, to mitigate heat stress damage at flowering in rice, O. sativa. J. Exp. Bot. 66, 1227 1236. Hoekenga, O.A., Vision, T.J., Shaff, J.E., Monforte, A.J., Lee, G.P., Howell, S.H., et al., 2003. Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta 3 Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol. 132, 936 948. Available from: https://doi.org/10.1104/pp.103.023085.worldwide. Hofman, G., Van Cleemput, O., 2004. Soil and Plant Nitrogen. International Fertilizer Industry Association Paris. Honsdorf, N., March, T.J., Berger, B., Tester, M., Pillen, K., 2014a. High-throughput phenotyping to detect drought tolerance QTL in wild barley introgression lines. PLoS One 9 (5), e97047. Honsdorf, N., March, T.J., Hecht, A., Eglinton, J., Pillen, K., 2014b. Evaluation of juvenile drought stress tolerance and genotyping by sequencing with wild barley introgression lines. Mol. Breed. 34 (3), 1475 1495. Hossain, H., Rahman, M., Alam, M., Singh, R., 2015. Mapping of quantitative trait loci associated with reproductive-stage salt tolerance in rice. J. Agron. Crop Sci. 201, 17 31. Hu, B., Wu, P., Liao, C.Y., Zhang, W.P., Ni, J.J., 2001. QTLs and epistasis underlying activity of acid phosphatase under phosphorus sufficient and deficient condition in rice (Oryza sativa L.). Plant Soil 230 (1), 99 105. Available from: https://doi.org/10.1023/A:1004809525119. Hund, A., Fracheboud, Y., Soldati, A., Frascaroli, E., Salvi, S., Stamp, P., 2004. QTL controlling root and shoot traits of maize seedlings under cold stress. TAG Theor. Appl. Genet. 109, 618 629. Idrissi, O., Udupa, S.M., De Keyser, E., McGee, R.J., Coyne, C.J., Saha, G.C., et al., 2016. Identification of quantitative trait loci controlling root and shoot traits associated with drought tolerance in a lentil (Lens culinaris Medik.) recombinant inbred line population. Front. Plant Sci. 7, 1174. Ikka, T., Kobayashi, Y., Tazib, T., Koyama, H., 2008. Aluminum-tolerance QTL in Columbia/Kashmir inbred population of Arabidopsis thaliana is not associated with aluminum-responsive malate excretion. Plant Sci. 175 (4), 533 538. Available from: https://doi.org/10.1016/j.plantsci.2008.06.001. Induri, B.R., Ellis, D.R., Slavov, G.T., Yin, T., Zhang, X., Muchero, W., et al., 2012. Identification of quantitative trait loci and candidate genes for cadmium tolerance in Populus. Tree Physiol. 32 (5), 626 638. Available from: https://doi.org/10.1093/treephys/tps032. Jagadish, S.V.K., Cairns, J., Lafitte, R., Wheeler, T.R., Price, A.H., Craufurd, P.Q., 2010. Genetic analysis of heat tolerance at anthesis in rice all rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher. Crop Sci. 50, 1633 1641. Jefferies, S.P., Pallotta, M.A., Paull, J.G., Karakousis, A., Kretschmer, J.M., Manning, S., et al., 2000. Mapping and validation of chromosome regions conferring boron toxicity tolerance in wheat (Triticum aestivum). TAG Theor. Appl. Genet. 101 (5 6), 767 777. Available from: https://doi.org/10.1007/s001220051542. Jenni, S., Truco, M.J., Michelmore, R.W., 2013. Quantitative trait loci associated with tipburn, heat stress-induced physiological disorders, and maturity traits in crisphead lettuce. TAG Theor. Appl. Genet. 126, 3065 3079. Jermstad, K.D., Bassoni, D.L., Wheeler, N.C., Anekonda, T.S., Aitken, S.N., Adams, W.T., et al., 2001. Mapping of quantitative trait loci controlling adaptive traits in coastal Douglas-fir. II. Spring and fall cold-hardiness. TAG Theor. Appl. Genet. 102, 1152 1158. Jespersen, D., Merewitz, E., Xu, Y., Honig, J., Bonos, S., Meyer, W., et al., 2016. Quantitative trait loci associated with physiological traits for heat tolerance in creeping bentgrass. Crop Sci. 56, 1314 1329. Ji, S.L., Jiang, L., Wang, Y.H., Zhang, W.W., Liu, X., Liu, S.J., et al., 2009. Quantitative trait loci mapping and stability for low temperature germination ability of rice. Plant Breed. 128, 387 392. Jiang, L., Liu, S., Hou, M., Tang, J., Chen, L., Zhai, H., et al., 2006. Analysis of QTLs for seed low temperature germinability and anoxia germinability in rice (Oryza sativa L.). Field Crops Res. 98 (1), 68 75. Available from: https://doi.org/10.1016/j.fcr.2005.12.015. John Goodstal, F., Kohler, G.R., Randall, L.B., Bloom, A.J., St Clair, D.A., 2005. A major QTL introgressed from wild Lycopersicon hirsutum confers chilling tolerance to cultivated tomato (Lycopersicon esculentum). TAG Theor. Appl. Genet. 111, 898 905.

Plant Life under Changing Environment

952

38. Use of quantitative trait loci to develop stress tolerance in plants

Juenger, T.E., Mckay, J.K., Hausmann, N., Stowe, K.A., Dawson, T.E., Simms, E.L., et al., 2005. Identification and characterization of QTL underlying whole plant physiology in Arabidopsis thaliana: d13C, stomatal conductance and transpiration efficiency. Plant Cell Environ. 28 (6), 697 708. Available from: https://doi.org/10.1111/ j.1365-3040.2004.01313.x. Kalladan, R., Worch, S., Rolletschek, H., Harshavardhan, V.T., Kuntze, L., Seiler, C., et al., 2013. Identification of quantitative trait loci contributing to yield and seed quality parameters under terminal drought in barley advanced backcross lines. Mol. Breed. 32 (1), 71 90. Kamoshita, A., Wade, L.J., Ali, M.L., Pathan, M.S., Zhang, J., Sarkarung, S., et al., 2002. Mapping QTLs for root morphology of a rice population adapted to rainfed lowland conditions. TAG Theor. Appl. Genet. 104 (5), 880 893. Available from: https://doi.org/10.1007/s00122-001-0837-5. Kan, G., Ning, L., Li, Y., Hu, Z., Zhang, W., He, X., et al., 2016. Identification of novel loci for salt stress at the seed germination stage in soybean. Breed. Sci. 66, 530 541. Kassem, M.A., Meksem, K., Kang, C.H., Njiti, V.N., Kilo, V., Wood, A.J., et al., 2004. Loci underlying resistance to manganese toxicity mapped in a soybean recombinant inbred line population of “Essex” 3 “Forrest”. Plant Soil 260 (1 2), 197 204. Available from: https://doi.org/10.1023/B:PLSO.0000030189.96115.21. Kato, Y., Hirotsu, S., Nemoto, K., Yamagishi, J., 2008. Identification of QTLs controlling rice drought tolerance at seedling stage in hydroponic culture. Euphytica 160 (3), 423 430. Available from: https://doi.org/10.1007/ s10681-007-9605-1. Kebede, H., Subudhi, P.K., Rosenow, D.T., Nguyen, H.T., 2001. Quantitative trait loci influencing drought tolerance in grain sorghum (Sorghum bicolor L. Moench). TAG Theor. Appl. Genet. 103 (2 3), 266 276. Khabaz-Saberi, H., Graham, R.D., Pallotta, M.A., Rathjen, A.J., Williams, K.J., 2002. Genetic markers for manganese efficiency in durum wheat. Plant Breed. 121 (3), 224 227. Available from: https://doi.org/10.1046/ j.1439-0523.2002.00690.x. Kholova´, J., Nepolean, T., Hash, C.T., Supriya, A., Rajaram, V., Senthilvel, S., et al., 2012. Water saving traits comap with a major terminal drought tolerance quantitative trait locus in pearl millet [Pennisetum glaucum (L.) R. Br.]. Mol. Breed. 30 (3), 1337 1353. Khu, D.M., Reyno, R., Han, Y., Zhao, P.X., Bouton, J.H., Brummer, E.C., et al., 2013. Identification of aluminum tolerance quantitative trait loci in tetraploid alfalfa. Crop Sci. 53 (1), 148 163. Available from: https://doi.org/ 10.2135/cropsci2012.03.0181. Kiani, S.P., Grieu, P., Maury, P., Hewezi, T., Gentzbittel, L., Sarrafi, A., 2007. Genetic variability for physiological traits under drought conditions and differential expression of water stress-associated genes in sunflower (Helianthus annuus L.). TAG Theor. Appl. Genet. 114 (2), 193 207. Kindu, G.A., Tang, J., Yin, X., Struik, P.C., 2014. Quantitative trait locus analysis of nitrogen use efficiency in barley (Hordeum vulgare L.). Euphytica 199 (1 2), 207 221. Available from: https://doi.org/10.1007/s10681-014-1138-9. Klein, M.A., Lo´pez-Milla´n, A.-F., Grusak, M.A., 2012. Quantitative trait locus analysis of root ferric reductase activity and leaf chlorosis in the model legume, Lotus japonicus. Plant Soil 351 (1 2), 363 376. Available from: https://doi.org/10.1007/s11104-011-0972-y. Klein, A., Houtin, H., Rond, C., Marget, P., Jacquin, F., Boucherot, K., et al., 2014. QTL analysis of frost damage in pea suggests different mechanisms involved in frost tolerance. TAG Theor. Appl. Genet. 127, 1319 1330. Knoll, J., Gunaratna, N., Ejeta, G., 2008. QTL analysis of early-season cold tolerance in sorghum. TAG Theor. Appl. Genet. 116, 577 587. Kobayashi, Y., Koyama, H., 2002. QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. Plant Cell Physiol. 43 (12), 1526 1533. Koide, Y., Pariasca Tanaka, J., Rose, T., Fukuo, A., Konisho, K., Yanagihara, S., et al., 2013. QTLs for phosphorus deficiency tolerance detected in upland NERICA varieties. Plant Breed. 132 (3), 259 265. Available from: https://doi.org/10.1111/pbr.12052. Kong, F.M., Guo, Y., Liang, X., Wu, C.H., Wang, Y.Y., Zhao, Y., et al., 2013. Potassium (K) effects and QTL mapping for K efficiency traits at seedling and adult stages in wheat. Plant Soil 373 (1 2), 877 892. Available from: https://doi.org/10.1007/s11104-013-1844-4. Kooyers, N.J., 2015. The evolution of drought escape and avoidance in natural herbaceous populations. Plant Sci. 234, 155 162. Koyama, M.L., Levesley, A., Koebner, R.M.D., Flowers, T.J., Yeo, A.R., 2001. Quantitative trait loci for component physiological traits determining salt tolerance in rice. Plant Physiol. 125, 406 422.

Plant Life under Changing Environment

References

953

Kreps, J.A., Wu, Y., Chang, H.S., Zhu, T., Wang, X., Harper, J.F., 2002. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130 (4), 2129 2141. Krupa, Z., 1988. Cadmium-induced changes in the composition and structure of the light-harvesting complex II in radish cotyledons. Physiol. Plant. 73, 518 524. Kumar, U., Joshi, A.K., Kumari, M., Paliwal, R., Kumar, S., Ro¨der, M.S., 2010. Identification of QTLs for stay green trait in wheat (Triticum aestivum L.) in the ‘Chirya 3’ 3 ‘Sonalika’ population. Euphytica 174 (3), 437 445. Kuroki, M., Saito, K., Matsuba, S., Yokogami, N., Shimizu, H., Ando, I., et al., 2007. A quantitative trait locus for cold tolerance at the booting stage on rice chromosome 8. TAG Theor. Appl. Genet. 115, 593 600. Lanaras, T., Moustakas, M., Symenoidis, L., Diamantoglou, S., Karataglis, S., 1993. Plant metal content, growth responses and some photosynthetic measurements on field-cultivated wheat growing on ore bodies enriched in Cu. Physiol. Plant. 88, 307 314. 88, 307 317. Landi, P., Giuliani, S., Salvi, S., Ferri, M., Tuberosa, R., Sanguineti, M.C., 2010. Characterization of root-yield-1.06, a major constitutive QTL for root and agronomic traits in maize across water regimes. J. Exp. Bot. 61 (13), 3553 3562. Landi, M., Remorini, D., Pardossi, A., Guidi, L., 2013. Boron excess affects photosynthesis and antioxidant apparatus of greenhouse Cucurbita pepo and Cucumis sativus. J. Plant Res. 126 (6), 775 786. Langridge, P., Reynolds, M.P., 2015. Genomic tools to assist breeding for drought tolerance. Curr. Opin. Biotechnol. 32, 130 135. Laperche, A., Le Gouis, J., Hanocq, E., Brancourt-Hulmel, M., 2008. Modelling nitrogen stress with probe genotypes to assess genetic parameters and genetic determinism of winter wheat tolerance to nitrogen constraint. Euphytica 161 (1 2), 259 271. Available from: https://doi.org/10.1007/s10681-007-9433-3. Larsen, P.B., Tai, C.Y., Kochian, L.V., Howell, S.H., 1996. Arabidopsis mutants with increased sensitivity to aluminum. Plant Physiol. 110 (3), 743 751. Available from: https://doi.org/10.1104/pp.110.3.743. Larsen, P.B., Degenhardt, J., Tai, C.Y., Stenzler, L.M., Howell, S.H., Kochian, L.V., 1998. Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol. 117, 9 18. Available from: https://doi.org/10.1104/pp.117.1.9. Lee, G.J., Boerma, H.R., Villagarcia, M.R., Zhou, X., Carter, T.E., Li, Z., et al., 2004. A major QTL conditioning salt tolerance in s-100 soybean and descendent cultivars. TAG Theor. Appl. Genet. 109, 1610 1619. Lee, J.-S., Sajise, A.G.C., Gregorio, G.B., Kretzschmar, T., Ismail, A.M., Wissuwa, M., 2017. Genetic dissection for zinc deficiency tolerance in rice using bi-parental mapping and association analysis. TAG Theor. Appl. Genet. 130 (9), 1903 1914. Available from: https://doi.org/10.1007/s00122-017-2932-2. Lejeune-He´naut, I., Hanocq, E., Be´thencourt, L., Fontaine, V., Delbreil, B., Morin, J., et al., 2008. The flowering locus Hr colocalizes with a major QTL affecting winter frost tolerance in Pisum sativum L. TAG Theor. Appl. Genet. 116, 1105 1116. Li, M., Guo, X., Zhang, M., Wang, X., Zhang, G., Tian, Y., et al., 2010. Mapping QTLs for grain yield and yield components under high and low phosphorus treatments in maize (Zea mays L.). Plant Sci. 178 (5), 454 462. Available from: https://doi.org/10.1016/j.plantsci.2010.02.019. Li, Y., Gu, M., Zhang, X., Zhang, J., Fan, H., Li, P., et al., 2014a. Engineering a sensitive visual-tracking reporter system for real-time monitoring phosphorus deficiency in tobacco. Plant Biotechnol. J. 12 (6), 674 684. Li, Z., Mei, S., Mei, Z., Liu, X., Fu, T., Zhou, G., et al., 2014b. Mapping of QTL associated with waterlogging tolerance and drought resistance during the seedling stage in oilseed rape (Brassica napus). Euphytica 197 (3), 341 353. Available from: https://doi.org/10.1007/s10681-014-1070-z. Li, P., Chen, F., Cai, H., Liu, J., Pan, Q., Liu, Z., et al., 2015a. A genetic relationship between nitrogen use efficiency and seedling root traits in maize as revealed by QTL analysis. J. Exp. Bot. 66 (11), 3175 3188. Available from: https://doi.org/10.1093/jxb/erv127. Li, X., Alarco´n-Zu´n˜iga, B., Kang, J., Nadeem Tahir, M.H., Jiang, Q., Wei, Y., et al., 2015b. Mapping fall dormancy and winter injury in tetraploid alfalfa. Crop Sci. 55, 1995 2011. Li, N., Sun, J., Wang, J., Liu, H., Zheng, H., Yang, L., et al., 2017. QTL analysis for alkaline tolerance of rice and verification of a major QTL. Plant Breed. 136, 881 891. Lian, X., Xing, Y., Yan, H., Xu, C., Li, X., Zhang, Q., 2005. QTLs for low nitrogen tolerance at seedling stage identified using a recombinant inbred line population derived from an elite rice hybrid. TAG Theor. Appl. Genet. 112 (1), 85 96. Available from: https://doi.org/10.1007/s00122-005-0108-y.

Plant Life under Changing Environment

954

38. Use of quantitative trait loci to develop stress tolerance in plants

Liang, Q., Cheng, X., Mei, M., Yan, X., Liao, H., 2010. QTL analysis of root traits as related to phosphorus efficiency in soybean. Ann. Bot. 106 (1), 223 234. Available from: https://doi.org/10.1093/aob/mcq097. Liang, J.-L., Qu, Y.-P., Yang, C.-G., Ma, X.-D., Cao, G.-L., Zhao, Z.-W., et al., 2015. Identification of QTLs associated with salt or alkaline tolerance at the seedling stage in rice under salt or alkaline stress. Euphytica 201, 441 452. Liao, H., Yan, X., Rubio, G., Beebe, S.E., Blair, M.W., Lynch, J.P., 2004. Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct. Plant Biol. 31 (10), 959. Available from: https://doi.org/10.1071/FP03255. Lilley, J.M., Ludlow, M.M., McCouch, S.R., O’Toole, J.C.C., 1996. Locating QTL for osmotic adjustment and dehydration tolerance in rice. J. Exp. Bot. 47 (302), 1427 1436. Available from: https://doi.org/10.1093/jxb/ 47.9.1427. Lin, S.F., Grant, D., Cianzio, S., Shoemaker, R., 2000a. Molecular characterization of iron deficiency chlorosis in soybean. J. Plant Nutr. 23 (11 12), 1929 1939. Available from: https://doi.org/10.1080/01904160009382154. Lin, S.F., Baumer, J., Ivers, D., Cianzio, S., Shoemaker, R., 2000b. Nutrient solution screening of Fe chlorosis resistance in soybean evaluated by molecular characterization. J. Plant Nutr. 23 (11 12), 1915 1928. Available from: https://doi.org/10.1080/01904160009382153. Lin, H.X., Zhu, M.Z., Yano, M., Gao, J.P., Liang, Z.W., Su, W.A., et al., 2004. QTLs for Na 1 and K 1 uptake of the shoots and roots controlling rice salt tolerance. TAG Theor. Appl. Genet. 108, 253 260. Lindsay, M.P., Lagudah, E.S., Hare, R.A., Munns, R., 2004. A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct. Plant Biol. 31, 1105 1114. Liu, Y., Subhash, C., Yan, J., Song, C., Zhao, J., Li, J., 2011. Maize leaf temperature responses to drought: thermal imaging and quantitative trait loci (QTL) mapping. Environ. Exp. Bot. 71 (2), 158 165. Liu, X., Mak, M., Babla, M., Wang, F., Chen, G., Veljanoski, F., et al., 2014. Linking stomatal traits and expression of slow anion channel genes HvSLAH1 and HvSLAC1 with grain yield for increasing salinity tolerance in barley. Front. Plant Sci. 5, 634. Liu, W., Lu, T., Li, Y., Pan, X., Duan, Y., Min, J., et al., 2015. Mapping of quantitative trait loci for cold tolerance at the early seedling stage in landrace rice Xiang 743. Euphytica 201, 401 409. Loneragan, J.F., 1968. Nutrient requirements of plants. Nature 220 (5174), 1307. Long, N.V., Dolstra, O., Malosetti, M., Kilian, B., Graner, A., Visser, R.G.F., et al., 2013. Association mapping of salt tolerance in barley (Hordeum vulgare L.). TAG Theor. Appl. Genet. 126, 2335 2351. Lopes, M.S., Reynolds, M.P., 2012. Stay-green in spring wheat can be determined by spectral reflectance measurements (normalized difference vegetation index) independently from phenology. J. Exp. Bot. 63, 3789 3798. Lou, Q., Chen, L., Sun, Z., Xing, Y., Li, J., Xu, X., et al., 2007. A major QTL associated with cold tolerance at seedling stage in rice (Oryza sativa L.). Euphytica 158, 87 94. Lou, Q., Chen, L., Mei, H., Wei, H., Feng, F., Wang, P., et al., 2015. Quantitative trait locus mapping of deep rooting by linkage and association analysis in rice. J. Exp. Bot. 66 (15), 4749 4757. Available from: https://doi. org/10.1093/jxb/erv246. Lucas, M.R., Ehlers, J.D., Huynh, B.-L., Diop, N.-N., Roberts, P.A., Close, T.J., 2013. Markers for breeding heattolerant cowpea. Mol. Breed. 31, 529 536. Luo, X.-D., Liu, J., Dai, L.-F., Zhang, F.-T., Wan, Y., Xie, J.-K., 2017. Linkage map construction and QTL identification of P-deficiency tolerance in Oryza rufipogon Griff. at early seedling stage. Euphytica 213 (4), 96. Available from: https://doi.org/10.1007/s10681-017-1884-6. Ma, J.F., Shen, R.F., Zhao, Z.Q., Wissuwa, M., Takeuchi, Y., Ebitani, T., et al., 2002. Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol. 43 (6), 652 659. Available from: https://doi.org/10.1093/pcp/pcf081. Ma, H.X., Bai, G.H., Carver, B.F., Zhou, L.L., 2005. Molecular mapping of a quantitative trait locus for aluminum tolerance in wheat cultivar Atlas 66. TAG Theor. Appl. Genet. 112 (1), 51 57. Available from: https://doi. org/10.1007/s00122-005-0101-5. Ma, H.X., Bai, G.H., Lu, W.Z., 2006. Quantitative trait loci for aluminum resistance in wheat cultivar Chinese spring. Plant Soil 283 (1 2), 239 249. Available from: https://doi.org/10.1007/s11104-0060008-1. Ma, L., Zhou, E., Huo, N., Zhou, R., Wang, G., Jia, J., 2007. Genetic analysis of salt tolerance in a recombinant inbred population of wheat (Triticum aestivum L.). Euphytica 153, 109 117.

Plant Life under Changing Environment

References

955

Maathuis, F.J., Sanders, D., 1996. Mechanisms of potassium absorption by higher plant roots. Physiol. Plant. 96 (1), 158 168. Manangkil, O.E., Vu, H.T.T., Mori, N., Yoshida, S., Nakamura, C., 2013. Mapping of quantitative trait loci controlling seedling vigor in rice (Oryza sativa L.) under submergence. Euphytica 192, 63 75. Mano, Y., Muraki, M., Fujimori, M., Takamizo, T., Kindiger, B., 2005. Identification of QTL controlling adventitious root formation during flooding conditions in teosinte (Zea mays ssp. huehuetenangensis) seedlings. Euphytica 142 (1 2), 33 42. Available from: https://doi.org/10.1007/s10681-005-0449-2. Mano, Y., Omori, F., Takamizo, T., Kindiger, B., Bird, R.M., Loaisiga, C.H., et al., 2007. QTL mapping of root aerenchyma formation in seedlings of a maize x rare teosinte “Zea nicaraguensis” cross. Plant Soil 295 (1 2), 103 113. Available from: https://doi.org/10.1007/s11104-007-9266-9. Mao, D., Yu, L., Chen, D., Li, L., Zhu, Y., Xiao, Y., et al., 2015. Multiple cold resistance loci confer the high cold tolerance adaptation of Dongxiang wild rice (Oryza rufipogon) to its high-latitude habitat. TAG Theor. Appl. Genet. 128, 1359 1371. Marr, C. W., 1994. “Hydroponic Systems,” in Greenhouse Vegetable Production (Kansas State University). Mason, R.E., Mondal, S., Beecher, F.W., Pacheco, A., Jampala, B., Ibrahim, A.M.H., et al., 2010. QTL associated with heat susceptibility index in wheat (Triticum aestivum L.) under short-term reproductive stage heat stress. Euphytica 174, 423 436. Meissner, M., Orsini, E., Ruschhaupt, M., Melchinger, A.E., Hincha, D.K., Heyer, A.G., 2013. Mapping quantitative trait loci for freezing tolerance in a recombinant inbred line population of Arabidopsis thaliana accessions tenela and c24 reveals reveille1 as negative regulator of cold acclimation. Plant Cell Environ. 36, 1256 1267. Meng, L., Wang, B., Zhao, X., Ponce, K., Qian, Q., Ye, G., 2017. Association mapping of ferrous, zinc, and aluminum tolerance at the seedling stage in indica rice using MAGIC populations. Front. Plant Sci. 8 (October), 1 15. Available from: https://doi.org/10.3389/fpls.2017.01822. Messmer, R., Fracheboud, Y., Ba¨nziger, M., Stamp, P., Ribaut, J.M., 2011. Drought stress and tropical maize: QTLs for leaf greenness, plant senescence, and root capacitance. Field Crops Res. 124 (1), 93 103. Miftahudin, Scoles, G.J., Gustafson, J.P., 2002. AFLP markers tightly linked to the aluminum-tolerance gene Alt 3 in rye (Secale cereale L.). TAG Theor. Appl. Genet. 104 (4), 626 631. Available from: https://doi.org/10.1007/ s00122-001-0782-3. Miles, C.M., Wayne, M., 2008. Quantitative trait locus (QTL) analysis. Nat. Educ. 1, 1 7. Mitchell, J.H., Zulkafli, S.L., Bosse, J., Campbell, B., Snell, P., Mace, E.S., et al., 2016. Rice-cold tolerance across reproductive stages. Crop Pasture Sci. 67, 823 833. Mommer, L., Visser, E.J., 2005. Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Ann. Bot. 96 (4), 581 589. Morgan, J.M., Tan, M.K., 1996. Chromosomal location of a wheat osmoregulation gene using RFLP analysis. Aust. J. Plant Physiol. 23 (6), 803 806. Available from: https://doi.org/10.1071/PP9960803. Moya, J., Ros, R., Picazo, I., 1993. Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution in rice plants. Photosynth. Res. 36, 75 80. Nable, R.O., Ban˜uelos, G.S., Paull, J.G., 1997. Boron toxicity. Plant Soil 193 (August), 181 198. Available from: https://doi.org/10.1104/pp.110.158832. Nambara, E., Kuchitsu, K., 2011. Opening a new era of ABA research. J. Plant Res. 124, 431 435. Available from: https://doi.org/10.1007/s10265-011-0437-7. Nandi, S., Subudhi, P.K., Senadhira, D., Manigbas, N.L., Sen-Mandi, S., Huang, N., 1997. Mapping QTLs for submergence tolerance in rice by AFLP analysis and selective genotyping. Mol. Gen. Genet. 255 (1), 1 8. Available from: https://doi.org/10.1007/s004380050468. Narasimhamoorthy, B., Bouton, J.H., Olsen, K.M., Sledge, M.K., 2007. Quantitative trait loci and candidate gene mapping of aluminum tolerance in diploid alfalfa. TAG Theor. Appl. Genet. 114 (5), 901 913. Available from: https://doi.org/10.1007/s00122-006-0488-7. Navakode, S., Weidner, A., Lohwasser, U., Ro¨der, M.S., Bo¨rner, A., 2009. Molecular mapping of quantitative trait loci (QTLs) controlling aluminium tolerance in bread wheat. Euphytica 166 (2), 283 290. Available from: https://doi.org/10.1007/s10681-008-9845-8. Nguyen, V.T., Burow, M.D., Nguyen, H.T., Le, B.T., Le, T.D., Paterson, A.H., 2001. Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). TAG Theor. Appl. Genet. 102 (6 7), 1002 1010. Available from: https://doi.org/10.1007/s001220000472.

Plant Life under Changing Environment

956

38. Use of quantitative trait loci to develop stress tolerance in plants

Nguyen, V.L., Ribot, S.A., Dolstra, O., Niks, R.E., Visser, R.G.F., van der Linden, C.G., 2013. Identification of quantitative trait loci for ion homeostasis and salt tolerance in barley (Hordeum vulgare L.). Mol. Breed. 31, 137 152. Nounjan, N., Siangliw, J.L., Toojinda, T., Chadchawan, S., Theerakulpisut, P., 2016. Salt-responsive mechanisms in chromosome segment substitution lines of rice (Oryza sativa L. Cv. Kdml105). Plant Physiol. Biochem. 103, 96 105. Obata, H., 1995. Micro essential elements. In: Matsuo, A. (Ed.), Science of Rice Plant, second ed. Food and Agriculture Policy Research Center, Tokyo, Japan, pp. 402 419. , et. Ochiai, K., Uemura, S., Shimizu, A., Okumoto, Y., Matoh, T., 2008. Boron toxicity in rice (Oryza sativa L.). I. Quantitative trait locus (QTL) analysis of tolerance to boron toxicity. TAG Theor. Appl. Genet. 117 (1), 125 133. Available from: https://doi.org/10.1007/s00122-008-0758-7. Oluoch, G., Zheng, J., Wang, X., Khan, M.K.R., Zhou, Z., Cai, X., et al., 2016. QTL mapping for salt tolerance at seedling stage in the interspecific cross of Gossypium tomentosum with Gossypium hirsutum. Euphytica 209, 223 235. Padmaja, K., Prasad, D., Prasad, A., 1990. Inhibition of chlorophyll synthesis in Phaseolus vulgaris seedlings by cadmium acetate. Photosynthetica 24, 399 405. Pallotta, M.A., Graham, R.D., Langridge, P., Sparrow, D.H.B., Barker, S.J., 2000. RFLP mapping of manganese efficiency in barley. TAG Theor. Appl. Genet. 101 (7), 1100 1108. Available from: https://doi.org/10.1007/ s001220051585. Pandit, E., Tasleem, S., Barik, S.R., Mohanty, D.P., Nayak, D.K., Mohanty, S.P., et al., 2017. Genome-wide association mapping reveals multiple QTLs governing tolerance response for seedling stage chilling stress in indica rice. Front. Plant Sci. 8, 552. Parelle, J., Zapater, M., Scotti-Saintagne, C., Kremer, A., Jolivet, Y., Dreyer, E., et al., 2007. Quantitative trait loci of tolerance to waterlogging in a European oak (Quercus robur L.): Physiological relevance and temporal effect patterns. Plant Cell Environ. 30 (4), 422 434. Available from: https://doi.org/10.1111/j.13653040.2006.01629.x. Paul, P.J., Samineni, S., Thudi, M., Sajja, S.B., Rathore, A., Das, R.R., et al., 2018. Molecular mapping of QTLs for heat tolerance in chickpea. Int. J. Mol. Sci. 19, 1 20. Pearson, A., Cogan, N.O.I., Baillie, R.C., Hand, M.L., Bandaranayake, C.K., Erb, S., et al., 2011. Identification of QTLs for morphological traits influencing waterlogging tolerance in perennial ryegrass (Lolium perenne L.). TAG Theor. Appl. Genet. 122 (3), 609 622. Available from: https://doi.org/10.1007/s00122-010-1473-8. Pelleschi, S., Guy, S., Kim, J.Y., Pointe, C., Mahe´, A., Barthes, L., et al., 1999. Ivr2, a candidate gene for a QTL of vacuolar invertase activity in maize leaves. Gene-specific expression under water stress. Plant Mol. Biol. 39 (2), 373 380. Available from: https://doi.org/10.1023/A:1006116310463. Peng, Z., Liu, F., Wang, L., Zhou, H., Paudel, D., Tan, L., et al., 2017. Transcriptome profiles reveal gene regulation of peanut (Arachis hypogaea L.) nodulation. Sci. Rep. 7, 40066. Pinto, R.S., Lopes, M.S., Collins, N.C., Reynolds, M.P., 2016. Modelling and genetic dissection of staygreen under heat stress. Theor. Appl. Genet. 129, 2055 2074. Portis, E., Cericola, F., Barchi, L., Toppino, L., Acciarri, N., Pulcini, L., et al., 2015. Association mapping for fruit, plant and leaf morphology traits in eggplant. PLoS One 10 (8), e0135200. Prathet, P., Somta, P., Srinives, P., 2012. Mapping QTL conferring resistance to iron deficiency chlorosis in mungbean [Vigna radiata (L.) Wilczek]. Field Crops Res. 137, 230 236. Available from: https://doi.org/10.1016/J. FCR.2012.08.002. Presterl, T., Ouzunova, M., Schmidt, W., Mo¨ller, E.M., Ro¨ber, F.K., Knaak, C., et al., 2007. Quantitative trait loci for early plant vigour of maize grown in chilly environments. TAG Theor. Appl. Genet. 114, 1059 1070. Price, A.H., Steele, K.A., Moore, B.J., Jones, R.G.W., 2002. Upland rice grown in soil filled chambers and exposed to contrasting water-deficit regimes: mapping QTLs for root morphology and distribution. Field Crops Res. 76, 25 43. Ps, S., Sv, A.M., Prakash, C., Mk, R., Tiwari, R., Mohapatra, T., et al., 2017. High resolution mapping of QTLs for heat tolerance in rice using a 5K SNP array. Rice (New York, N.Y.) 10, 28. Qiu, F., Zheng, Y., Zhang, Z., Xu, S., 2007. Mapping of QTL associated with waterlogging tolerance during the seedling stage in maize. Ann. Bot. 99 (6), 1067 1081. Available from: https://doi.org/10.1093/aob/mcm055. Qiu, B., Zhou, W., Xue, D., Zeng, F., Ali, S., Zhang, G., 2010. Identification of Cr-tolerant lines in a rice (Oryza sativa) DH population. Euphytica 174 (2), 199 207. Available from: https://doi.org/10.1007/s10681-009-0115-1.

Plant Life under Changing Environment

References

957

Qiu, H., Mei, X., Liu, C., Wang, J., Wang, G., Wang, X., et al., 2013. Fine mapping of quantitative trait loci for acid phosphatase activity in maize leaf under low phosphorus stress. Mol. Breed. 32 (3), 629 639. Available from: https://doi.org/10.1007/s11032-013-9895-z. Qiu, H., Liu, C., Yu, T., Mei, X., Wang, G., Wang, J., et al., 2014. Identification of QTL for acid phosphatase activity in root and rhizosphere soil of maize under low phosphorus stress. Euphytica 197 (1), 133 143. Available from: https://doi.org/10.1007/s10681-013-1058-0. Qiu, X., Yuan, Z., Liu, H., Xiang, X., Yang, L., He, W., et al., 2015. Identification of salt tolerance-improving quantitative trait loci alleles from a salt-susceptible rice breeding line by introgression breeding. Plant Breed. 134, 653 660. Qu, C., Gong, X., Liu, C., Hong, M., Wang, L., Hong, F., 2012. Effects of manganese deficiency and added cerium on photochemical efficiency of maize chloroplasts. Biol. Trace Elem. Res. 146 (1), 94 100. Quan, R., Wang, J., Hui, J., Bai, H., Lyu, X., Zhu, Y., et al., 2018. Improvement of salt tolerance using wild rice genes. Front. Plant Sci. 8, 2269. Quarrie, S.A., Gulli, M., Calestani, C., Steed, A., Marmiroli, N., 1994. Location of a gene regulating droughtinduced abscisic acid production on the long arm of chromosome 5A of wheat. TAG Theor. Appl. Genet. 89 (6), 794 800. Available from: https://doi.org/10.1007/BF00223721. Quero, G., Gutı´errez, L., Lascano, R., Monza, J., Sandal, N., Borsani, O., 2014. Identification of QTLs for shoot and root growth under ionic osmotic stress in lotus, using a RIL population. Crop Pasture Sci. 65, 139 149. Quesada, V.C., Garcı´a-Martı´nez, S., Piqueras, P., Ponce, M.A.R., Micol, J.L., 2002. Genetic architecture of NaCl tolerance in Arabidopsis. Plant Physiol. 130, 951 963. Raghothama, K.G., Karthikeyan, A.S., 2005. Phosphate acquisition. Plant Soil 274 (1 2), 37 49. Available from: https://doi.org/10.1007/s11104-004-2005-6. Raman, H., Moroni, J.S., Sato, K., Read, B.J., Scott, B.J., 2002. Identification of AFLP and microsatellite markers linked with an aluminium tolerance gene in barley (Hordeum vulgare L.). TAG Theor. Appl. Genet. 105 (2 3), 458 464. Available from: https://doi.org/10.1007/s00122-002-0934-0. Ravi, K., Vadez, V., Isobe, S., Mir, R.R., Guo, Y., Nigam, S.N., et al., 2011. Identification of several small maineffect QTLs and a large number of epistatic QTLs for drought tolerance related traits in groundnut (Arachis hypogaea L.). TAG Theor. Appl. Genet. 122 (6), 1119 1132. Available from: https://doi.org/10.1007/s00122010-1517-0. Ray, I.M., Han, Y., Lei, E., Meenach, C.D., Santantonio, N., Sledge, M.K., et al., 2015. Identification of quantitative trait loci for alfalfa forage biomass productivity during drought stress. Crop Sci. 55 (5), 2012 2033. Available from: https://doi.org/10.2135/cropsci2014.12.0840. Rehman, A.U., Malhotra, R.S., Bett, K., Tar’an, B., Bueckert, R., Warkentin, T.D., 2011. Mapping QTL associated with traits affecting grain yield in chickpea (Cicer arietinum L.) under terminal drought stress. Crop Sci. 51 (2), 450 463. Available from: https://doi.org/10.2135/cropsci2010.03.0129. Rerkasem, B., 1996. Boron and plant reproductive development. In: Sterility in Wheat in Subtropical Asia: Extent, Causes and Solutions, vol. 72. pp. 32 34. Reymond, M., Svistoonoff, S., Loudet, O., Nussaume, L., Desnos, T., 2006. Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ. 29 (1), 115 125. Available from: https://doi.org/10.1111/j.1365-3040.2005.01405.x. Reyna, N., Cornelious, B., Shannon, J.G., Sneller, C.H., 2003. Evaluation of a QTL for waterlogging tolerance in southern soybean germplasm. Crop Sci. 43 (6), 2077 2082. Available from: https://doi.org/10.2135/ cropsci2003.2077. Riede, C.R., Anderson, J.A., 1996. Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Sci. 36 (4), 905 909. Available from: https://doi.org/10.2135/cropsci1996.0011183X0036000400015x. Rodrı´guez, V.M., Butro´n, A., Rady, M.O.A., Soengas, P., Revilla, P., 2014. Identification of quantitative trait loci involved in the response to cold stress in maize (Zea mays L.). Mol. Breed. 33, 363 371. Ruta, N., Liedgens, M., Fracheboud, Y., Stamp, P., Hund, A., 2010. QTLs for the elongation of axile and lateral roots of maize in response to low water potential. TAG Theor. Appl. Genet. 120 (3), 621 631. Ryan, P.R., Ditomaso, J.M., Kochian, L.V., 1993. Aluminum toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44, 437 446. Ryan, P.R., Liao, M., Delhaize, E., Rebetzke, G.J., Weligama, C., Spielmeyer, W., et al., 2015. Early vigour improves phosphate uptake in wheat. J. Exp. Bot. 66 (22), 7089 7100. Available from: https://doi.org/10.1093/jxb/erv403.

Plant Life under Changing Environment

958

38. Use of quantitative trait loci to develop stress tolerance in plants

Saito, K., Miura, K., Nagano, K., Hayano-Saito, Y., Araki, H., Kato, A., 2001. Identification of two closely linked quantitative trait loci for cold tolerance on chromosome 4 of rice and their association with anther length. TAG Theor. Appl. Genet. 103, 862 868. Sallam, A., Arbaoui, M., El-Esawi, M., Abshire, N., Martsch, R., 2016. Identification and verification of QTL associated with frost tolerance using linkage mapping and GWAS in winter faba bean. Front. Plant Sci. 7, 1098. Sanchez, A.C., Subudhi, P.K., Rosenow, D.T., Nguyen, H.T., 2002. Mapping QTLs associated with drought resistance in sorghum (Sorghum bicolor L. Moench). Plant Mol. Biol. 48 (5 6), 713 726. Sanguineti, M.C., Tuberosa, R., Landi, P., Salvi, S., Maccaferri, M., Casarini, E., et al., 1999. QTL analysis of drought related traits and grain yield in relation to genetic variation for leaf abscisic acid concentration in field-grown maize. J. Exp. Bot. 50 (337), 1289 1297. Available from: https://doi.org/10.1093/jxb/50.337.1289. Saranga, Y.E., Jiang, C.X., Wright, R.J., Yakir, D., Paterson, A.H., 2004. Genetic dissection of cotton physiological responses to arid conditions and their inter-relationships with productivity. Plant Cell Environ. 27 (3), 263 277. Savci, S., 2012. Investigation of effect of chemical fertilizers on environment. Apcbee Procedia 1, 287 292. Schneider, K., 2005. Mapping populations and principles of genetic mapping. In: Meksem, K., Kahl, G. (Eds.), The Handbook of Plant Genome Mapping: Genetic and Physical Mapping. (Wiley-VCH Verlag GmbH & Co. KGaA), pp. 1 21. Available from: https://doi.org/10.1002/3527603514.ch1. Septiningsih, E.M., Sanchez, D.L., Singh, N., Sendon, P.M.D., Pamplona, A.M., Heuer, S., et al., 2012. Identifying novel QTLs for submergence tolerance in rice cultivars IR72 and Madabaru. Theor. Appl. Genet. 124, 867 874. Sharma, A.D., Sharma, H., Lightfoot, D.A., 2011. The genetic control of tolerance to aluminum toxicity in the “Essex” by “Forrest” recombinant inbred line population. TAG Theor. Appl. Genet. 122 (4), 687 694. Available from: https://doi.org/10.1007/s00122-010-1478-3. Sharma, D., Singh, R., Rane, J., Gupta, V.K., Mamrutha, H.M., Tiwari, R., et al., 2016. Mapping quantitative trait loci associated with grain filling duration and grain number under terminal heat stress in bread wheat (Triticum aestivum L.). Plant Breed. 135, 538 545. Sharma, D.K., Torp, A.M., Rosenqvist, E., Ottosen, C.-O., Andersen, S.B., 2017. QTLs and potential candidate genes for heat stress tolerance identified from the mapping populations specifically segregating for Fv/Fm in wheat. Front. Plant Sci. 8, 1668. Shimizu, A., Yanagihara, S., Kawasaki, S., Ikehashi, H., 2004. Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). TAG Theor. Appl. Genet. 109 (7), 1361 1368. Available from: https://doi.org/ 10.1007/s00122-004-1751-4. Shirasawa, K., Sekii, T., Ogihara, Y., Yamada, T., Shirasawa, S., Kishitani, S., et al., 2013. Identification of the chromosomal region responsible for high-temperature stress tolerance during the grain-filling period in rice. Mol. Breed. 32, 223 232. Siangliw, M., Toojinda, T., Tragoonrung, S., Vanavichit, A., 2003. Thai jasmine rice carrying QTLch9 (Sub QTL) is submergence tolerant. Ann. Bot. 91, 255 261. Sivaguru, M., Paliwal, K., 1993. Differential aluminum tolerance in some tropical rice cultivars. II. Mechanism of aluminum tolerance. J. Plant Nutr. 16 (9), 1717 1732. ˝ Skinner, J.S., Szucs, P., von Zitzewitz, J., Marquez-Cedillo, L., Filichkin, T., Stockinger, E.J., et al., 2006. Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. TAG Theor. Appl. Genet. 112, 832 842. Sledge, M.K., Bouton, J.H., Dall’Agnoll, M., Parrottb, W.A., Kochertc, G., 2002. Identification and confirmation of aluminum tolerance QTL in diploid Medicago sativa subsp. coerulea. Crop Sci. 42 (4), 1121 1128. Available from: https://doi.org/10.2135/cropsci2002.1121. Sledge, M.K., Ray, I.M., Jiang, G., 2005. An expressed sequence tag SSR map of tetraploid alfalfa (Medicago sativa L.). TAG Theor. Appl. Genet. 111 (5), 980 992. Available from: https://doi.org/10.1007/s00122-005-0038-8. Specht, J.E., Chase, K., Macrander, M., Graef, G.L., Chung, J., Markwell, J.P., et al., 1986. Cell biology & molecular genetics soybean response to water: a QTL analysis of drought tolerance. Crop Sci. 41, 493 509. Available from: https://doi.org/10.2135/cropsci2001.412493x. Srinives, P., Kitsanachandee, R., Chalee, T., Sommanas, W., Chanprame, S., 2010. Inheritance of resistance to iron deficiency and identification of AFLP markers associated with the resistance in mungbean (Vigna radiata (L.) Wilczek). Plant Soil 335 (1 2), 423 437. Available from: https://doi.org/10.1007/s11104-010-0431-1. Sripongpangkul, K., Posa, G.B.T., Senadhira, D.W., Brar, D., Huang, N., Khush, G.S., et al., 2000. Genes/QTLs affecting flood tolerance in rice. TAG Theor. Appl. Genet. 101 (7), 1074 1081. Available from: https://doi. org/10.1007/s001220051582.

Plant Life under Changing Environment

References

959

Stadtman, T., 1990. Selenium biochemistry. Annu. Rev. Biochem. 59, 111 127. St Burgos, M., Messmer, M.M., Stamp, P., Schmid, J.E., 2001. Flooding tolerance of spelt (Triticum spelta L.) compared to wheat (Triticum aestivum L.)—a physiological and genetic approach. Euphytica 122 (2), 287 295. Available from: https://doi.org/10.1023/A:1012945902299. Steele, K.A., Price, A.H., Shashidhar, H.E., Witcombe, J.R., 2006. Marker-assisted selection to introgress rice QTLs controlling root traits into an Indian upland rice variety. TAG Theor. Appl. Genet. 112 (2), 208 221. Available from: https://doi.org/10.1007/s00122-005-0110-4. Stinchcombe, J., Hoekstra, H., 2008. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100, 158 170. Available from: https://doi.org/10.1038/sj. hdy.6800937. Stobart, A., Griyths, W., Ameen-Bukhari, I., Sherwood, R., 1985. The eVect of Cd21 on the biosynthesis of chlorophyll of barley. Physiol. Plant. 63, 293 298. Strigens, A., Freitag, N.M., Gilbert, X., Grieder, C., Riedelsheimer, C., Schrag, T.A., et al., 2013. Association mapping for chilling tolerance in elite flint and dent maize inbred lines evaluated in growth chamber and field experiments. Plant Cell Environ. 36, 1871 1887. Su, J., Xiao, Y., Li, M., Liu, Q., Li, B., Tong, Y., et al., 2006. Mapping QTLs for phosphorus-deficiency tolerance at wheat seedling stage. Plant Soil 281 (1 2), 25 36. Available from: https://doi.org/10.1007/s11104-005-3771-5. Su, J.-Y., Zheng, Q., Li, H.-W., Li, B., Jing, R.-L., Tong, Y.-P., et al., 2009. Detection of QTLs for phosphorus use efficiency in relation to agronomic performance of wheat grown under phosphorus sufficient and limited conditions. Plant Sci. 176 (6), 824 836. Available from: https://doi.org/10.1016/J.PLANTSCI.2009.03.006. Su, J., Zhang, F., Li, P., Guan, Z., Fang, W., Chen, F., 2016. Genetic variation and association mapping of waterlogging tolerance in chrysanthemum. Planta 244 (6), 1241 1252. Available from: https://doi.org/10.1007/s00425016-2583-6. Suh, J.P., Lee, C.K., Lee, J.H., Kim, J.J., Kim, S.M., Cho, Y.C., et al., 2012. Identification of quantitative trait loci for seedling cold tolerance using RILs derived from a cross between japonica and tropical japonica rice cultivars. Euphytica 184, 101 108. Sumner, M.E., Fey, M.V., Noble, A.D., 1991. Nutrient status and toxicity problems in acid soils. Soil Acidity. Springer, Berlin, Heidelberg, pp. 149 182. Takai, T., Ohsumi, A., San-Oh, Y., Laza, M.R.C., Kondo, M., Yamamoto, T., et al., 2009. Detection of a quantitative trait locus controlling carbon isotope discrimination and its contribution to stomatal conductance in japonica rice. TAG Theor. Appl. Genet. 118 (7), 1401 1410. Available from: https://doi.org/10.1007/s00122009-0990-9. Takehisa, H., Shimodate, T., Fukuta, Y., Ueda, T., Yano, M., Yamaya, T., et al., 2004. Identification of quantitative trait loci for plant growth of rice in paddy field flooded with salt water. Field Crops Res. 89, 85 95. Takeuchi, Y., Hayasaka, H., Chiba, B., Tanaka, I., Shimano, T., Yamagishi, M., et al., 2001. Mapping quantitative trait loci controlling cool-temperature tolerance at booting stage in temperate japonica rice. Breed. Sci. 51, 191 197. Tang, Y., Sorrells, M.E., Kochian, L.V., Garvin, D.F., 2000. Identification of RFLP markers linked to the barley aluminum tolerance gene Alp. Crop Sci. 40 (3), 778 782. Available from: https://doi.org/10.2135/ cropsci2000.403778x. Tao, Y.Z., Henzell, R.G., Jordan, D.R., Butler, D.G., Kelly, A.M., McIntyre, C.L., 2000. Identification of genomic regions associated with stay green in sorghum by testing RILs in multiple environments. TAG Theor. Appl. Genet. 100 (8), 1225 1232. Tazib, T., Ikka, T., Kuroda, K., Kobayashi, Y., Kimura, K., Koyama, H., 2009. Quantitative trait loci controlling resistance to cadmium rhizotoxicity in two recombinant inbred populations of Arabidopsis thaliana are partially shared by those for hydrogen peroxide resistance. Physiol. Plant. 136 (4), 395 406. Available from: https:// doi.org/10.1111/j.1399-3054.2009.01234.x. Tazib, T., Kobayashi, Y., Koyama, H., Matsui, T., 2015. QTL analyses for anther length and dehiscence at flowering as traits for the tolerance of extreme temperatures in rice (Oryza sativa L.). Euphytica 203, 629 642. Teng, S., Tian, C., Chen, M., Zeng, D., Guo, L., Zhu, L., et al., 2006. QTLs and candidate genes for chlorate resistance in rice (Oryza sativa L.). Euphytica 152, 141 148. Teulat, B., This, D., Khairallah, M., Borries, C., Ragot, C., Sourdille, P., et al., 1998. Several QTLs involved in osmotic adjustment trait variation in barley (Hordeum vulgare L.). TAG Theor. Appl. Genet. 96 (5), 688 698.

Plant Life under Changing Environment

960

38. Use of quantitative trait loci to develop stress tolerance in plants

Thomas, H., Ougham, H., 2014. The stay-green trait. J. Exp. Bot. 65 (14), 3889 3900. Available from: https://doi. org/10.1093/jxb/eru037. Thomas, H., Smart, C.M., 1993. Crops that stay green 1. Ann. Appl. Biol. 123, 193 219. Thomas, H., Stoddart, J.L., 1975. Separation of chlorophyll degradation from other senescence processes in leaves of a mutant genotype of meadow fescue (Festuca pratensis L.). Plant Physiol. 56, 438 441. Tiwari, C., Wallwork, H., Kumar, U., Dhari, R., Arun, B., Mishra, V.K., et al., 2013. Molecular mapping of high temperature tolerance in bread wheat adapted to the eastern Gangetic plain region of India. Field Crops Res. 154, 201 210. Trapp, J.J., Urrea, C.A., Zhou, J., Khot, L.R., Sankaran, S., Miklas, P.N., 2016. Selective phenotyping traits related to multiple stress and drought response in dry bean. Crop Sci. 56 (4), 1460 1472. Tripathy, J.N., Zhang, J., Robin, S., Nguyen, T.T., Nguyen, H.T., 2000. QTLs for cell-membrane stability mapped in rice (Oryza sativa L.) under drought stress. TAG Theor. Appl. Genet. 100, 1197 1202. Truco, M.J., Randall, L.B., Bloom, A.J., St Clair, D.A., 2000. Detection of QTLs associated with shoot wilting and root ammonium uptake under chilling temperatures in an interspecific backcross population from Lycopersicon esculentum 3 l. Hirsutum. TAG Theor. Appl. Genet. 101, 1082 1092. Tsarouhas, V., Gullberg, U., Lagercrantz, U., 2004. Mapping of quantitative trait loci (QTLs) affecting autumn freezing resistance and phenology in salix. TAG Theor. Appl. Genet. 108, 1335 1342. Tuberosa, R., Sanguineti, M.C., Landi, P., Salvi, S., Casarini, E., Conti, S., 1998. RFLP mapping of quantitative trait loci controlling abscisic acid concentration in leaves of drought-stressed maize (Zea mays L.). TAG Theor. Appl. Genet. 97 (5 6), 744 755. Available from: https://doi.org/10.1007/s001220050951. Tuberosa, R., Sanguineti, M.C., Landi, P., Giuliani, M.M., Salvi, S., Conti, S., 2002. Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol. Biol. 48 (5 6), 697 712. Tuinstra, M.R., Grote, E.M., Goldsbrough, P.B., Ejeta, G., 1997. Genetic analysis of post-flowering drought tolerance and components of grain development in Sorghum bicolor (L.) Moench. Mol. Breed 3, 439 448. Tumino, G., Voorrips, R.E., Rizza, F., Badeck, F.W., Morcia, C., Ghizzoni, R., et al., 2016. Population structure and genome-wide association analysis for frost tolerance in oat using continuous SNP array signal intensity ratios. Theor. Appl. Genet. 129, 1711 1724. Turner, N.C., 2018. Turgor maintenance by osmotic adjustment: 40 years of progress. J. Exp. Bot. 69 (13), 3223 3233. Tuyen, D.D., Lal, S.K., Xu, D.H., 2010. Identification of a major QTL allele from wild soybean (Glycine soja sieb. & zucc.) for increasing alkaline salt tolerance in soybean. TAG Theor. Appl. Genet. 121, 229 236. Tuyen, D.D., Zhang, H.M., Xu, D.H., 2013. Validation and high-resolution mapping of a major quantitative trait locus for alkaline salt tolerance in soybean using residual heterozygous line. Mol. Breed. 31, 79 86. Tyrka, M., Rapacz, M., Fiust, A., Wo´jcik-Jagła, M., Rognli, O.A., 2015. Quantitative trait loci mapping of freezing tolerance and photosynthetic acclimation to cold in winter two- and six-rowed barley. Plant Breed. 134, 271 282. Uga, Y., Okuno, K., Yano, M., 2011. Dro1, a major QTL involved in deep rooting of rice under upland field conditions. J. Exp. Bot. 62 (8), 2485 2494. Available from: https://doi.org/10.1093/jxb/erq429. Ul Haq, T., Gorham, J., Akhtar, J., Akhtar, N., Steele, K.A., 2010. Dynamic quantitative trait loci for salt stress components on chromosome 1 of rice. Funct. Plant Biol. 37, 634 645. Upadhyaya, H.D., Kashiwagi, J., Varshney, R.K., Gaur, P.M., Saxena, K.B., Krishnamurthy, L., et al., 2012. Phenotyping chickpeas and pigeonpeas for adaptation to drought. Front. Physiol. 3, 179. Vadez, V., Krishnamurthy, L., Thudi, M., Anuradha, C., Colmer, T.D., Turner, N.C., et al., 2012. Assessment of ICCV 2 3 JG 62 chickpea progenies shows sensitivity of reproduction to salt stress and reveals QTL for seed yield and yield components. Mol. Breed. 30, 9 21. Van Nguyen, L., Takahashi, R., Githiri, S.M., Rodriguez, T.O., Tsutsumi, N., Kajihara, S., et al., 2017. Mapping quantitative trait loci for root development under hypoxia conditions in soybean (Glycine max L. Merr.). TAG Theor. Appl. Genet. 130 (4), 743 755. Available from: https://doi.org/10.1007/s00122-016-2847-3. Varshney, R.K., Thudi, M., Nayak, S.N., Gaur, P.M., Kashiwagi, J., Krishnamurthy, L., et al., 2014. Genetic dissection of drought tolerance in chickpea (Cicer arietinum L.). TAG Theor. Appl. Genet. 127 (2), 445 462. Varshney, R.K., Tuberosa, R., Tardieu, F., 2018a. Progress in understanding drought tolerance: from alleles to cropping systems. J. Exp. Bot. 69 (13), 3175 3179.

Plant Life under Changing Environment

References

961

Varshney, R.K., Thudi, M., Pandey, M.K., Tardieu, F., Ojiewo, C., Vadez, V., et al., 2018b. Accelerating genetic gains in legumes for the development of prosperous smallholder agriculture: integrating genomics, phenotyping, systems modelling and agronomy. J. Exp. Bot. 69 (13), 3293 3312. Villalta, I., Bernet, G.P., Carbonell, E.A., Asins, M.J., 2007. Comparative QTL analysis of salinity tolerance in terms of fruit yield using two Solanum populations of F7 lines. TAG Theor. Appl. Genet. 114, 1001 1017. Villalta, I., Reina-Sa´nchez, A., Boları´n, M.C., Cuartero, J., Belver, A., Venema, K., et al., 2008. Genetic analysis of Na 1 and K 1 concentrations in leaf and stem as physiological components of salt tolerance in tomato. TAG Theor. Appl. Genet. 116, 869 880. Wan, J., Zhai, H., Wan, J., Ikehashi, H., 2003. Detection and analysis of QTLs for ferrous iron toxicity tolerance in rice, Oryza sativa L. Genome Res. 131 (2), 201 206. Available from: https://doi.org/10.1023/ A:1023915710103. Wang, Y.X., Wu, P., Wu, Y.R., Yan, X.L., 2002. Molecular marker analysis of manganese toxicity tolerance in rice under greenhouse conditions. Plant Soil 238 (2), 227 233. Available from: https://doi.org/10.1023/ A:1014487428033. Wang, J., McClean, P.E., Lee, R., Goos, R.J., Helms, T., 2008. Association mapping of iron deficiency chlorosis loci in soybean (Glycine max L. Merr.) advanced breeding lines. TAG Theor. Appl. Genet. 116 (6), 777 787. Available from: https://doi.org/10.1007/s00122-008-0710-x. Wang, J., Drayton, M.C., George, J., Cogan, N.O.I., Baillie, R.C., Hand, M.L., et al., 2010. Identification of genetic factors influencing salt stress tolerance in white clover (Trifolium repens L.) by QTL analysis. TAG Theor. Appl. Genet. 120, 607 619. Wang, Z., Wang, F., Zhou, R., Wang, J., Zhang, H., 2011a. Identification of quantitative trait loci for cold tolerance during the germination and seedling stages in rice (Oryza sativa L.). Euphytica 181, 405. Wang, Z., Wang, J., Bao, Y., Wu, Y., Zhang, H., 2011b. Quantitative trait loci controlling rice seed germination under salt stress. Euphytica 178, 297 307. Wang, Y., Sun, S., Liu, B., Wang, H., Deng, J., Liao, Y., et al., 2011c. A sequence-based genetic linkage map as a reference for Brassica rapa pseudochromosome assembly. BMC Genomics 12 (1), 239. Available from: https:// doi.org/10.1186/1471-2164-12-239. Wang, Z., Cheng, J., Chen, Z., Huang, J., Bao, Y., Wang, J., et al., 2012. Identification of QTLs with main, epistatic and QTL 3 environment interaction effects for salt tolerance in rice seedlings under different salinity conditions. TAG Theor. Appl. Genet. 125, 807 815. Wang, S., Cao, M., Ma, X., Chen, W., Zhao, J., Sun, C., et al., 2017. Integrated RNA sequencing and QTL mapping to identify candidate genes from Oryza rufipogon associated with salt tolerance at the seedling stage. Front. Plant Sci. 8. Weber, C.A., Moore, G.A., Deng, Z., Gmitter, F.G., 2003. Mapping freeze tolerance quantitative trait loci in a Citrus grandis 3 Poncirus trifoliata F1 pseudo-testcross using molecular markers. J. Am. Soc. Hortic. Sci. 128, 508 514. Wei, Z., Julkowska, M.M., Laloe¨, J.-O., Hartman, Y., de Boer, G.-J., Michelmore, R.W., et al., 2014. A mixed-model QTL analysis for salt tolerance in seedlings of crop-wild hybrids of lettuce. Mol. Breed. 34, 1389 1400. Welcker, C., Boussuge, B., Bencivenni, C., Ribaut, J.M., Tardieu, F., 2006. Are source and sink strengths genetically linked in maize plants subjected to water deficit? A QTL study of the responses of leaf growth and of anthesis-silking interval to water deficit. J. Exp. Bot. 58 (2), 339 349. Wight, C.P., Kibite, S., Tinker, N.A., Molnar, S.J., 2006. Identification of molecular markers for aluminium tolerance in diploid oat through comparative mapping and QTL analysis. TAG Theor. Appl. Genet. 112 (2), 222 231. Available from: https://doi.org/10.1007/s00122-005-0114-0. Wissuwa, M., Ae, N., 2001. Further characterization of two QTLs that increase phosphorus uptake of rice (Oryza sativa L.) under phosphorus deficiency. Plant Soil 237 (2), 275 286. Available from: https://doi.org/10.1023/ A:1013385620875. Wissuwa, M., Wegner, J., Ae, N., Yano, M., 2002. Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. TAG Theor. Appl. Genet. 105 (6 7), 890 897. Available from: https://doi.org/10.1007/s00122-002-1051-9. Wissuwa, M., Ismail, A.M., Yanagihara, S., 2006. Effects of zinc deficiency on rice growth and genetic factors contributing to tolerance. Plant Physiol. 142 (2), 731 741. Available from: https://doi.org/10.1104/pp.106.085225. Wu, P., Liao, C.Y., Hu, B., Yi, K.K., Jin, W.Z., Ni, J.J., et al., 2000. QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. TAG Theor. Appl. Genet. 100 (8), 1295 1303.

Plant Life under Changing Environment

962

38. Use of quantitative trait loci to develop stress tolerance in plants

Wu, J., Yuan, Y.-X., Zhang, X.-W., Zhao, J., Song, X., Li, Y., et al., 2008. Mapping QTLs for mineral accumulation and shoot dry biomass under different Zn nutritional conditions in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Plant Soil 310 (1 2), 25 40. Available from: https://doi.org/10.1007/s11104-008-9625-1. Xia, J., Yamaji, N., Che, J., Shen, R.F., Ma, J.F., 2014. Differential expression of Nrat1 is responsible for Altolerance QTL on chromosome 2 in rice. J. Exp. Bot. 65 (15), 4297 4304. Available from: https://doi.org/ 10.1093/jxb/eru201. Xiao, Y., Pan, Y., Luo, L., Zhang, G., Deng, H., Dai, L., et al., 2011. Quantitative trait loci associated with seed set under high temperature stress at the flowering stage in rice (Oryza sativa L.). Euphytica 178, 331 338. Xiao, N., Huang, W.-N., Zhang, X.-X., Gao, Y., Li, A.-H., Dai, Y., et al., 2014. Fine mapping of qRC10-2, a quantitative trait locus for cold tolerance of rice roots at seedling and mature stages. PLoS One 9, e96046. Xiao, N., Huang, W.-N., Li, A.-H., Gao, Y., Li, Y.-H., Pan, C.-H., et al., 2015. Fine mapping of the qLOP2 and qPSR2-1 loci associated with chilling stress tolerance of wild rice seedlings. TAG Theor. Appl. Genet. 128, 173 185. Xie, Y., Sun, X., Ren, J., Fan, J., Lou, Y., Fu, J., et al., 2015. Genetic diversity and association mapping of cadmium tolerance in bermudagrass [Cynodon dactylon (L.) Pers.]. Plant Soil 390 (1 2), 307 321. Available from: https://doi.org/10.1007/s11104-015-2391-y. Xu, K., Xu, X., Ronald, P.C., Mackill, D.J., 2000a. A high-resolution linkage map of the vicinity of the rice submergence tolerance locus Sub1. Mol. Gen. Genet. 263 (4), 681 689. Available from: https://doi.org/10.1007/ s004380051217. Xu, W., Subudhi, P.K., Crasta, O.R., Rosenow, D.T., Mullet, J.E., Nguyen, H.T., 2000b. Molecular mapping of QTLs conferring stay-green in grain sorghum (Sorghum bicolor L. Moench). Genome 43 (3), 461 469. Xu, F.S., Wang, Y.H., Meng, J., 2001. Mapping boron efficiency gene(s) in Brassica napus using RFLP and AFLP markers. Plant Breed. 120 (4), 319 324. Available from: https://doi.org/10.1046/j.1439-0523.2001.00583.x. Xu, L.-M., Zhou, L., Zeng, Y.-W., Wang, F.-M., Zhang, H.-L., Shen, S.-Q., et al., 2008. Identification and mapping of quantitative trait loci for cold tolerance at the booting stage in a japonica rice near-isogenic line. Plant Sci. 174, 340 347. Xu, Y.-F., An, D.-G., Liu, D.-C., Zhang, A.-M., Xu, H.-X., Li, B., 2012. Mapping QTLs with epistatic effects and QTL 3 treatment interactions for salt tolerance at seedling stage of wheat. Euphytica 186, 233 245. Xu, Y., Li, S., Li, L., Zhang, X., Xu, H., An, D., et al., 2013. Mapping QTLs for salt tolerance with additive, epistatic and QTL 3 treatment interaction effects at seedling stage in wheat. Plant Breed. 132, 276 283. Xue, Y., Wan, J.M., Jiang, L., Liu, L.L., Su, N., Zhai, H.Q., et al., 2006. QTL analysis of aluminum resistance in rice (Oryza sativa L.). Plant Soil 287 (1 2), 375 383. Available from: https://doi.org/10.1007/s11104-006-9086-3. Xue, D., Chen, M., Zhang, G., 2009a. Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica 165 (3), 587 596. Available from: https://doi.org/ 10.1007/s10681-008-9785-3. Xue, D., Huang, Y., Zhang, X., Wei, K., Westcott, S., Li, C., et al., 2009b. Identification of QTLs associated with salinity tolerance at late growth stage in barley. Euphytica 169, 187 196. Yadav, R., Courtois, B., Huang, N., McLaren, G., 1997. Mapping genes controlling root morphology and root distribution in adoubled-haploid population of rice. TAG Theor. Appl. Genet. 94, 619 632. Yadav, R.S., Hash, C.T., Bidinger, F.R., Cavan, G.P., Howarth, C.J., 2002. Quantitative trait loci associated with traits determining grain and stover yield in pearl millet under terminal drought-stress conditions. TAG Theor. Appl. Genet. 104 (1), 67 83. Yan, X., Liao, H., Beebe, S.E., Blair, M.W., Lynch, J.P., 2004. QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265 (1 2), 17 29. Available from: https://doi.org/10.1007/s11104-005-0693-1. Yang, J., Sears, R.G., Gill, B.S., Paulsen, G.M., 2002. Quantitative and molecular characterization of heat tolerance in hexaploid wheat. Euphytica 126, 275 282. Yang, M., Ding, G., Shi, L., Feng, J., Xu, F., Meng, J., 2010. Quantitative trait loci for root morphology in response to low phosphorus stress in Brassica napus. TAG Theor. Appl. Genet. 121 (1), 181 193. Available from: https://doi.org/10.1007/s00122-010-1301-1. Yang, L.M., Liu, H.L., Lei, L., Zhao, H.W., Wang, J.G., Li, N., et al., 2017. Identification of QTLs controlling low-temperature germinability and cold tolerance at the seedling stage in rice (Oryza sativa L.). Euphytica 214, 13.

Plant Life under Changing Environment

References

963

Ye, C., Fukai, S., Godwin, I.D., Koh, H., Reinke, R., Zhou, Y., et al., 2010. A QTL controlling low temperature induced spikelet sterility at booting stage in rice. Euphytica 176, 291 301. Ye, C., Argayoso, M.A., Redon˜a, E.D., Sierra, S.N., Laza, M.A., Dilla, C.J., et al., 2012. Mapping QTL for heat tolerance at flowering stage in rice using SNP markers. Plant Breed. 131, 33 41. Ye, C., Tenorio, F.A., Redon˜a, E.D., Morales Cortezano, P.S., Cabrega, G.A., Jagadish, K.S.V., et al., 2015. Finemapping and validating qhtsf4.1 to increase spikelet fertility under heat stress at flowering in rice. TAG Theor. Appl. Genet. 128, 1507 1517. Yoshida, S., Ahn, J.S., Forno, D.A., 1973. Occurrence, diagnosis, and correction of zinc deficiency of lowland rice. Soil Sci. Plant Nutr. 19 (2), 83 93. Zeng, C., Xu, F., Wang, Y., Hu, C., Meng, J., 2007. Physiological basis of QTLs for boron efficiency in Arabidopsis thaliana. Plant Soil 296 (1 2), 187 196. Available from: https://doi.org/10.1007/s11104-007-9309-2. Zeng, C., Han, Y., Shi, L., Peng, L., Wang, Y., Xu, F., et al., 2008. Genetic analysis of the physiological responses to low boron stress in Arabidopsis thaliana. Plant Cell Environ. 31 (1). Available from: https://doi.org/10.1111/ j.1365-3040.2007.01745.x071115091544002-???. Zhang, H., Wang, H., 2015. QTL mapping for traits related to P-deficient tolerance using three related RIL populations in wheat. Euphytica 203 (3), 505 520. Available from: https://doi.org/10.1007/s10681-014-1248-4. Zhang, J., Zheng, H.G., Aarti, A., Pantuwan, G., Nguyen, T.T., Tripathy, J.N., et al., 2001. Locating genomic regions associated with components of drought resistance in rice: comparative mapping within and across species. TAG Theor. Appl. Genet. 103 (1), 19 29. Zhang, L.H., Abdel-Ghany, S.E., Freeman, J.L., Ackley, A.R., Schiavon, M., Pilon-Smits, E.A.H., 2006a. Investigation of selenium tolerance mechanisms in Arabidopsis thaliana. Physiol. Plant. 128 (2), 212 223. Available from: https://doi.org/10.1111/j.1399-3054.2006.00739.x. Zhang, L., Byrne, P.F., Pilon-Smits, E.A.H., 2006b. Mapping quantitative trait loci associated with selenate tolerance in Arabidopsis thaliana. New Phytol. 170 (1), 33 42. Available from: https://doi.org/10.1111/j.14698137.2006.01635.x. Zhang, D., Cheng, H., Geng, L., Kan, G., Cui, S., Meng, Q., et al., 2009. Detection of quantitative trait loci for phosphorus deficiency tolerance at soybean seedling stage. Euphytica 167 (3), 313 322. Available from: https:// doi.org/10.1007/s10681-009-9880-0. Zhang, D., Liu, C., Cheng, H., Kan, G., Cui, S., Meng, Q., et al., 2010. Quantitative trait loci associated with soybean tolerance to low phosphorus stress based on flower and pod abscission. Plant Breed. 129 (3), 243 249. Available from: https://doi.org/10.1111/j.1439-0523.2009.01682.x. Zhang, D., Song, H., Cheng, H., Hao, D., Wang, H., Kan, G., et al., 2014a. The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genetics 10 (1), e1004061. Available from: https://doi.org/10.1371/journal.pgen.1004061. Zhang, S., Zheng, J., Liu, B., Peng, S., Leung, H., Zhao, J., et al., 2014b. Identification of QTLs for cold tolerance at seedling stage in rice (Oryza sativa L.) using two distinct methods of cold treatment. Euphytica 195, 95 104. Zhang, P., Zhong, K., Tong, H., Shahid, M.Q., Li, J., 2016a. Association mapping for aluminum tolerance in a core collection of rice landraces. Front. Plant Sci. 7 (October), 1 11. Available from: https://doi.org/10.3389/ fpls.2016.01415. Zhang, D., Li, H., Wang, J., Zhang, H., Hu, Z., Chu, S., et al., 2016b. High-density genetic mapping identifies new major loci for tolerance to low-phosphorus stress in soybean. Front. Plant Sci. 7, 372. Available from: https:// doi.org/10.3389/fpls.2016.00372. Zhang, X., Zhou, G., Shabala, S., Koutoulis, A., Shabala, L., Johnson, P., et al., 2016c. Identification of aerenchyma formation-related QTL in barley that can be effective in breeding for waterlogging tolerance. TAG Theor. Appl. Genet. 129 (6), 1167 1177. Available from: https://doi.org/10.1007/s00122-016-2693-3. Zhang, X., Fan, Y., Shabala, S., Koutoulis, A., Shabala, L., Johnson, P., et al., 2017. A new major-effect QTL for waterlogging tolerance in wild barley (H. spontaneum). TAG Theor. Appl. Genet. 130 (8), 1559 1568. Available from: https://doi.org/10.1007/s00122-017-2910-8. Zhang, J., Zhang, S., Cheng, M., Jiang, H., Zhang, X., Peng, C., et al., 2018a. Effect of drought on agronomic traits of rice and wheat: a meta-analysis. Int. J. Environ. Res. Public Health 15 (5), 1 14. Zhang, Y., Anis, G.B., Wang, R., Wu, W., Yu, N., Shen, X., et al., 2018b. Genetic dissection of QTL against phosphate deficiency in the hybrid rice ‘Xieyou9308’. Plant Growth Regul. 84 (1), 123 133. Available from: https://doi.org/10.1007/s10725-017-0326-8.

Plant Life under Changing Environment

964

38. Use of quantitative trait loci to develop stress tolerance in plants

Zhao, Y., Gowda, M., Wu¨rschum, T., Longin, C.F.H., Korzun, V., Kollers, S., et al., 2013. Dissecting the genetic architecture of frost tolerance in central European winter wheat. J. Exp. Bot. 64, 4453 4460. Zhao, L., Zhao, C.-F., Zhou, L.-H., Lin, J., Zhao, Q.-Y., Zhu, Z., et al., 2016. QTL mapping of dehiscence length at the basal part of thecae related to heat tolerance of rice (Oryza sativa L.). Euphytica 209, 715 723. Zheng, H., Babu, M.R.C., Pathan, M.S., Ali, L., Huang, N., Courtois, B., et al., 2000. Quantitative trait loci for rootpenetration ability and root thickness in rice: comparison of genetic backgrounds. Genome 43 (1), 53 61. Available from: https://doi.org/10.1139/gen-43-1-53. Zheng, H.J., Wu, A.Z., Zheng, C.C., Wang, Y.F., Cai, R., Shen, X.F., et al., 2009. QTL mapping of maize (Zea mays) stay-green traits and their relationship to yield. Plant Breed. 128 (1), 54 62. Zhi-Hong, Z., Li, S., Wei, L., Wei, C., Ying-Guo, Z., 2005. A major QTL conferring cold tolerance at the early seedling stage using recombinant inbred lines of rice (Oryza sativa L.). Plant Sci. 168, 527 534. Zhou, L., Zeng, Y., Zheng, W., Tang, B., Yang, S., Zhang, H., et al., 2010. Fine mapping a QTL qctb7 for cold tolerance at the booting stage on rice chromosome 7 using a near-isogenic line. TAG Theor. Appl. Genet. 121, 895 905. Zhou, M., Johnson, P., Zhou, G., Li, C., Lance, R., 2012. Quantitative trait loci for waterlogging tolerance in a barley cross of franklin 3 YuYaoXiangTian Erleng and the relationship between waterlogging and salinity tolerance. Crop Sci. 52 (5), 2082 2088. Available from: https://doi.org/10.2135/cropsci2012.01.0008. Zhou, Z., Zhang, C., Lu, X., Wang, L., Hao, Z., Li, M., et al., 2018. Dissecting the genetic basis underlying combining ability of plant height related traits in maize. Front. Plant Sci. 9, 1117. Zhu, J., Kaeppler, S.M., Lynch, J.P., 2005. Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270 (1), 299 310. Available from: https://doi.org/10.1007/s11104004-1697-y. Zur, I., Krzewska, M., Dubas, E., Gołebiowska-Pikania, G., Janowiak, F., Stojałowski, S., 2012. Molecular mapping of loci associated with abscisic acid accumulation in triticale ( 3 Triticosecale Wittm.) anthers in response to low temperature stress inducing androgenic development. Plant Growth Regul. 68 (3), 483 492. Available from: https://doi.org/10.1007/s10725-012-9738-7.

Further reading Badri, M., Chardon, F., Huguet, T., Aouani, M.E., 2011. Quantitative trait loci associated with drought tolerance in the model legume Medicago truncatula. Euphytica 181 (3), 415. Bielenberg, D.G., Rauh, B., Fan, S., Gasic, K., Abbott, A.G., Reighard, G.L., et al., 2015. Genotyping by sequencing for SNP-based linkage map construction and QTL analysis of chilling requirement and bloom date in peach [Prunus persica (L.) Batsch]. PLoS One 1 14. Available from: https://doi.org/10.1371/journal. pone.0139406. Borrell, A.K., Mullet, J.E., George-Jaeggli, B., van Oosterom, E.J., Hammer, G.L., Klein, P.E., et al., 2014. Drought adaptation of stay-green sorghum is associated with canopy development, leaf anatomy, root growth, and water uptake. J. Exp. Bot. 65 (21), 6251 6263. Chloupek, O., Forster, B.P., Thomas, W.T., 2006. The effect of semi-dwarf genes on root system size in fieldgrown barley. TAG Theor. Appl. Genet. 112 (5), 779 786. Crasta, O.R., Xu, W.W., Rosenow, D.T., Mullet, J., Nguyen, H.T., 1999. Mapping of post-flowering drought resistance traits in grain sorghum: association between QTLs influencing premature senescence and maturity. Mol. Gen. Genet. MGG 262 (3), 579 588. El-Soda, M., Boer, M.P., Bagheri, H., Hanhart, C.J., Koornneef, M., Aarts, M.G., 2014. Genotype environment interactions affecting preflowering physiological and morphological traits of Brassica rapa grown in two watering regimes. J. Exp. Bot. 65 (2), 697 708. Gong, X., McDonald, G., 2017. QTL mapping of root traits in phosphorus-deficient soils reveals important genomic regions for improving NDVI and grain yield in barley. TAG Theor. Appl. Genet. 130 (9), 1885 1902. Hao, Z., Liu, X., Li, X., Xie, C., Li, M., Zhang, D., et al., 2009. Identification of quantitative trait loci for drought tolerance at seedling stage by screening a large number of introgression lines in maize. Plant Breed. 128 (4), 337 341. Haussmann, B., Mahalakshmi, V., Reddy, B., Seetharama, N., Hash, C., Geiger, H., 2002. QTL mapping of staygreen in two sorghum recombinant inbred populations. Theor. Appl. Genet. 106 (1), 133 142.

Plant Life under Changing Environment

Further reading

965

Hussain, W., Stephen Baenziger, P., Belamkar, V., Guttieri, M.J., Venegas, J.P., Easterly, A., et al., 2017. Genotyping-by-sequencing derived high-density linkage map and its application to QTL mapping of flag leaf traits in bread wheat. Sci. Rep. 7, 1 15. Available from: https://doi.org/10.1038/s41598-017-16006-z. Johnson, W.C., Jackson, L.E., Ochoa, O., Van Wijk, R., Peleman, J., Clair, D.S., et al., 2000. Lettuce, a shallowrooted crop, and Lactuca serriola, its wild progenitor, differ at QTL determining root architecture and deep soil water exploitation. Theor. Appl. Genet. 101 (7), 1066 1073. Kholova´, J., Hash, C.T., Koˇcova´, M., Vadez, V., 2011. Does a terminal drought tolerance QTL contribute to differences in ROS scavenging enzymes and photosynthetic pigments in pearl millet exposed to drought? Environ. Exp. Bot. 71 (1), 99 106. Merewitz, E., Belanger, F., Warnke, S., Huang, B., Bonos, S., 2014. Quantitative trait loci associated with drought tolerance in creeping bentgrass. Crop Sci. 54 (5), 2314 2324. Muchero, W., Ehlers, J.D., Roberts, P.A., 2010. Restriction site polymorphism-based candidate gene mapping for seedling drought tolerance in cowpea [Vigna unguiculata (L.) Walp.]. Theor. Appl. Genet. 120 (3), 509 518. Poormohammad Kiani, S., Grieu, P., Maury, P., Hewezi, T., Gentzbittel, L., Sarrafi, A., 2007. Genetic variability for physiological traits under drought conditions and differential expression of water stress-associated genes in sunflower (Helianthus annuus L.). Theor. Appl. Genet. 114 (2), 193 207. Available from: https://doi.org/ 10.1007/s00122-006-0419-7. Pootakham, W., Jomchai, N., Ruang-areerate, P., Shearman, J.R., Sonthirod, C., Sangsrakru, D., et al., 2015. Genome-wide SNP discovery and identification of QTL associated with agronomic traits in oil palm using genotyping-by-sequencing (GBS). Genomics 105, 288 295. Available from: https://doi.org/10.1016/j. ygeno.2015.02.002. Reynolds, M., Tuberosa, R., 2008. Translational research impacting on crop productivity in drought-prone environments. Curr. Opin. Plant Biol. 11 (2), 171 179. Available from: https://doi.org/10.1016/j.pbi.2008.02.005. Tisne, S., Schmalenbach, I., Reymond, M., Dauzat, M., Pervent, M., Vile, D., et al., 2010. Keep on growing under drought: genetic and developmental bases of the response of rosette area using a recombinant inbred line population. Plant Cell Environ. 33 (11), 1875 1887. Tondelli, A., Francia, E., Barabaschi, D., Aprile, A., Skinner, J.S., Stockinger, E.J., et al., 2006. Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor. Appl. Genet. 112 (3), 445 454. Toojinda, T., Siangliw, M., Tragoonrung, S., Vanavichit, A., 2003. Molecular genetics of submergence tolerance in rice: QTL analysis of key traits. Ann. Bot. 91 (SPEC. ISS. JAN.), 243 253. Available from: https://doi.org/10.1093/aob/mcf072. Verma, V., Foulkes, M.J., Worland, A.J., Sylvester-Bradley, R., Caligari, P.D.S., Snape, J.W., 2004. Mapping quantitative trait loci for flag leaf senescence as a yield determinant in winter wheat under optimal and droughtstressed environments. Euphytica 135 (3), 255 263.

Plant Life under Changing Environment

Index Note: Page numbers followed by “f” and “t” refer to figures and tables, respectively.

A ABA expression, 813 Abar/chlh/gun5 expression, 812 813 Abelmoschus esculentus, 29t Abiotic stress, 175 176, 398 399, 498, 543 544, 611 612, 614 615, 825 826, 883 affecting clock genes transcription, 816 817 economic effects of the most disturbed abiotic stress, 884 effects on sugarcane plants, 251 270 drought, 257 258 future prospects, 266 267 heat and cold stress, 252 254 mechanical injuries, stress produced by, 258 264 nutrition-related stresses, 254 255 salt stress, 255 257 sucrose synthesis and partitioning during abiotic stress, 264 266 impact on plant growth and metabolism, 578 581 induction of tolerance to, 300 304 management of, 889 890 in southeast Mediterranean Sea, 891 897 in medicinal plants, 663 680, 673t cold stress, 671 672 drought stress, tolerance to, 664 665 heat stress, 669 671 heavy metal stress, 672 673 increased resistance to, 663 664 resistance mechanism of medicinal and aromatic plants to temperature stress, 668 669 resistance to light stress and UV in medicinal plants, 665 668 salt stress, tolerance to, 665 microRNAs in, 722 723 nitric oxide sources under. See Nitric oxide sources under abiotic stress phytohormonal signaling under. See Phytohormonal signaling under abiotic stress and programmed cell death, 8 16 drought- and flooding-induced programmed cell death, 10 11 future perspectives, 16

heavy metal- and nanoparticle-induced programmed cell death, 13 16 high and low temperature induced programmed cell death, 9 salinity-induced programmed cell death, 12 ultraviolet-induced programmed cell death, 12 13 reactive oxygen species regulation in plant organelles during, 326 333 apoplasts, 331 332 chloroplasts, 328 329 mitochondria, 329 330 peroxisomes, 330 331 rhizospheric bacteria in, 870 874 roles of aquaporins in, 647 654 drought/desiccation stress, aquaporins in, 648 650 low temperature stress, aquaporins in, 651 652 salinity stress, aquaporins in, 650 651 trace element transport and heavy-metal toxicity, aquaporins in, 652 654 signaling roles of ROS in plants under, 339 343 ROS signal perception, 339 340 transduction and interaction of ROS signaling, 340 343 transcriptomic modifications by, 304 307 Abiotic stress, single-cell response to, 615 620 computational biology, 614 615 microelectrode ion flux estimation technique, 616 619 aluminum stress, 617 619 salt stress, 616 617 water deficit and oxygen deprivation, 617 single-cell genomic analysis, 619 620 Abiotic stress, types of, 918, 919f cold stress, 937 940 drought stress, 918 924 hormonal response under drought, 921 osmotic adjustment (OA), 922 root responses under drought, 922 923 water-use and photosynthetic activity under drought, 921 922 yield responses under drought, 923 924

967

968 Abiotic stress, types of (Continued) flooding/waterlogging/submergence tolerance, 942 943 heat stress, 936 937 mineral stress, 924 931 QTL related to macro-minerals, 925 929 QTL related to micro-nutrients, 929 931 mineral toxicity, 931 936 aluminum, 931 933 boron, 934 cadmium, 933 934 chromium, 935 copper, 936 iron, 934 935 manganese, 935 selenium, 934 zinc, 936 salinity stress, 940 942 stay-green, 943 Abiotic stress factors, 8, 779 Abiotic-stress tolerance, 577 610, 755 future prospects, 595 598 modeling and simulation in plant system dynamics, 589 593 coexpression networks, 592 593 gene regulatory networks, 592 gene-to-metabolite networks, 590 protein protein interaction networks, 590 591 transcriptional regulatory networks, 591 592 multiple “omics” data, integration of, 587 589 metabolomic proteomic, 588 589 transcriptomic metabolomic, 588 transcriptomic proteomic, 587 588 software and algorithms for plant systems biology, 593 595 data handling and analysis, 594 storage and maintenance of data and results, 594 595 visualization of plant omics data, 594 systems biology approaches for improvement of, 581 587 genomics, 581 583 interactomics, 586 587 metabolomics, 585 586 “omics” approaches, 587 proteomics, 584 585 transcriptomics, 583 584 ABNORMAL INFLORESCENCE MERISTEM 1 (AIM1), 553 554 ABP1 (AUXIN BINDING PROTEIN1), 407 408 biosynthesis, 400 402 signaling, 402

Index

Abscisic acid (ABA), 56, 85, 92, 167, 341 343, 398 400, 401f, 403f, 405, 437 438, 483 484, 499, 513 514, 527 528, 543 544, 545t, 548, 780, 844 845, 921 ABA-aldehyde oxidase (AAO), 527 528 ABA-hypersensitive DCAF1 (ABD1), 528 clock components, 812 813 -dependent expression, 844 845 -dependent signal transduction, 402 405 -independent pathway, 828 -independent signal transduction, 405 in regulating and responding to low water availability, 847 Abscisic acid responsive elements (ABREs), 591 592 ACC 7 synthase (ACS7) genes, 305 ACC deaminase production, 867 Acclimatization, 886 887 ACC oxidase (ACO), 552 553 ACO2, 305 ACC synthase (ACS), 552 553 ACC SYNTHASE 8 (ACS8) enzyme, 818 Acer saccharinum L. seedlings, 191 192 Acetobacter, 359 Acetolactate synthase (ALS), 242 Acetylations, 513 514, 519 520 Acetyl-CoA, 159 N-Acetyl-o-methylserotonin, 775 N-Acetylserotonin O-methyltransferase (ASMT), 776 777 Achromobacter, 867 Achromobacter piechaudii, 366, 871 872, 872t, 874 Achromobneter, 359 Acidithiobacillus ferrooxidans, 378 Acid phosphatases, release of, 144 145 Acinetobacter, 365 367, 867 Acinetobacter calcoaceticus, 359 361, 363, 872t Acinetobacter strain RSC7, 863t Aconitate hydratase, 330 ACX1, 553 554 ACX5, 553 554 Acyl CoA oxidase (ACX), 553 554 Adenosine 50-Phosphosulfate Reductase2 (APR2) gene, 838 839 Adenosine triphosphate (ATP), 77 78, 159 ADP-glucose pyrophosphorylase, 503 504 Aeluropus littoralis, 489 490 Aerenchyma cells, 161 163, 942 Aeromonas, 359 AFBs/TIR1 (AUXIN SIGNALING F-BOX PROTEINS/ TRANSPORT INHIBITOR RESPONSE 1), 407 408 AGAMOUS protein, 424 Agmatine, 482 483 Agmatine deiminase, 482 483

Index

Agrarian yield, 884 Agribusiness, 891 892 Agrobacterium, 866 867 Agrobacterium tumefaciens, 486 488, 866 867 Agrochemicals, 237 Agrostis stolonifera, 694 AHK2, 550 551 AHK3, 550 551 Alcaligenes, 863t, 867, 872t Alditols, 759 Alfalfa (Medicago sativa), 635, 932 Alfin1 TF, 826 827 Alkaline soils, 63 Alkaloids, 785 Allium cepa, 15t, 191 192, 565t Alnus formosana (Burkill) Makino, 336 337 Aloe vera, 665 α-amylase genes, 502 α-linolenic acid (α-LeA), 424, 553 554 Alpha radiation, 108 α-tocopherol contents, 564 ALTERED PHOSPHATE STARVATION RESPONSE1 (APSR1), 125 Alternative oxidase (AOX), 330 Aluminum, 559 toxicity, 931 933 Aluminum stress, 617 619 Alyssum bertolonii, 222 Alyssum species, 222 Amidoxime-reducing component (ARC), 736, 739 Amino acids, 77 78, 758 759 biosynthesis, 245 246 γ-amino-N-butyric acid (GABA), 758 759 proline, 758 1-Aminocyclopropane-1-carboxylate (ACC) deaminase, 60, 84 85, 370, 867 1-Aminocyclopropane-1-carboxylic acid (ACC), 165 166, 341 343, 413 Ammopiptanthus nanus, 759 760 Ananas comosus, 29t Anaplerotic pathway, 701 Aneurinibacillus aneurinilyticus, 863t Anoectochilus formosanus, 667 Anthocyanin, 564 Anti-ACC, 487t Antioxidant, 762 763, 780 Antioxidant capacity, 295 296 Antioxidant compounds induction by nanoparticles, 294 304 abiotic stress, induction of tolerance to, 300 304 antioxidant capacity, 295 296 enzyme compounds, 298 299 nonenzymatic compounds, 299 300

969

oxidative stress, 294 295 oxidative stress induced by nanoparticles, 296 297 Antioxidant defense system, 3 in response to herbicide treatment, 243 244 Antioxidant enzymes’ response of plants to drought, 87 88 Antioxidants involved in stress-induced regulation of ROS, 333 339, 334f enzymatic antioxidants, 334 337 nonenzymatic antioxidants, 337 339 Antioxidant system, 8, 26 27, 741 742 Antioxidative defense mechanism under water-deficit stress, 187 Antioxidative enzymes induced plant synthesis of, 366 induction of, 363 Antiviral proteins, 471 472 APETALA2 (AP2) gene, 721 722, 828 Aponogeton madagascariensis, 10t Apoplastic alkalization and reacidulation, 59 Apoplastic invertase, 426 428 Apoplasts, 331 332 Apple (Malus baccata), 781 APR2 gene, 838 839 APX (ascorbate peroxidase), 335 336 APX gene (APX1), 35 36 AQP1 gene, 651 AQP7 gene, 651 AQP gene, 652 Aquaglyceroporins (GLAs), 644 646 Aquaporins (AQPs), 191 192, 517, 643 662, 645t, 646f, 654f in abiotic stresses, 647 654 drought/desiccation stress, 648 650 low temperature stress, 651 652 salinity stress, 650 651 trace element transport and heavy-metal toxicity, 652 654 brief history of, 644 functional and structural significance in plants, 644 646 future perspectives, 654 655 water dynamics and, 647 Arabidopsis, 6 7, 57 58, 93, 164 165, 264 266, 405, 416, 423 425, 441, 470 471, 483 484, 498 500, 515 516, 549 550, 585 587, 590, 619 620, 644, 648 653, 689, 724, 738, 740 741, 744 745, 757, 761 763, 781 784, 795 796, 802, 813, 816 817, 830, 867 868 Arabidopsis BIN2, 412 Arabidopsis Hsp101, 35 36 Arabidopsis mutants, 406, 437 Arabidopsis P5CS1 activity, 56

970 Arabidopsis PIP1b gene, 654 655 Arabidopsis thaliana, 5, 10t, 11t, 12, 13t, 14t, 15t, 29t, 35 36, 82 83, 88, 110 113, 118, 126 128, 132 135, 141 145, 224 226, 241, 266, 293, 304 310, 330, 340, 364, 404, 416, 419, 471 472, 473t, 486 488, 487t, 500 501, 517, 581 583, 588 589, 724, 737 738, 762 763, 815 816, 827 828, 835 836 ACR2 (CDC25) in, 842 843 aluminum (Al)-tolerant mutants in, 931 932 boron efficiency coefficient (BEC) in, 930 Tsu-1 and Ts-1 of, 838 839 Arabidopsis thaliana BBX21 (AtBBX21), 695 696 Arachis hypogaea, 14t Arachis hypogea, 924 Arbuscular mycorrhizae (AM), 84 85, 278 in salt-affected soils, 61 Arbuscular mycorrhizae fungal (AMF), 128, 139 141 in low phosphate stress tolerance, 139 141 Arbuscular mycorrhizae plant association on plant growth, 61 62 AREB gene, 304 305 ARF (AUXIN RESPONSE FACTORS), 407 408 D-Arginine, 490 491 Arginine decarboxylase (ADC), 426 428, 482, 487t Argonaute (AGO) proteins, 470 472 arsB, 225 226 arsC, 225 226 Arsenate reductase (ACR), 842 Arsenic (As), 209t, 214 215, 225 226, 697 698 arsM gene, 225 226 arsR, 225 226 Artemisia annua L., 667 Arthrobacter, 356, 363 Arthrobacter globiformis, 863t Arthrobacter protophormiae, 359 361 Arthrobacter sp., 361, 872t Ascorbate, 323 326 Ascorbate peroxidase (APX), 4 5, 243 244, 485 486, 556, 740 742 Ascorbic acid (AsA), 243, 337 338, 666 Asteraceae, 222 Astragalus racemosus, 222 Astragalus sinicus, 139 141 Astrostole scabra, 694 AtADC2 gene, 485 486 AtHXK1-dependent pathway, 500 501 AtMKK1, 340 341 AtNCED3, 93 ATP-binding cassette (ABC) transporter, 226 AtPHT1;1 gene, 135 136 AtPHT3, 132 133 AtPIP1 gene, 649

Index

AtPIP2 gene, 649 AtPME41, 412 ATP sulfurylase 1, 838 839 Atriplex atacamensis, 191 192 Atriplex gmelini, 63 64 Atriplex lentiformis, 53 AtTPPD, 757 AUGUSTUS software, 594 Autochthonous bacteria, 84 85 Aux/IAA protein, 547 548 Auxin (AUX), 84 85, 118 119, 126, 398 399, 406, 408, 408f, 513 514, 526, 543 544, 547 548 biosynthesis, 406 407 signaling, 407 408 Auxin response factors (ARFs), 126, 547 548, 721 722 Avena sativa, 487t, 489 490 Azospirilla, 866 867 Azospirillum, 356, 359, 362 363, 365 366, 866 867 Azospirillum brasilense, 362, 364, 863t, 868 Azotobacter, 356 Azotobacter chroococcum CAZ3, 863t

B Bacillus, 356, 359, 362, 867, 870 Bacillus amylolequifaciens, 362 364 Bacillus aquimaris, 362 Bacillus aryabhattai MCC3374, 863t Bacillus cereus, 226, 863t, 871 Bacillus circulans, 378, 863t Bacillus edaphicus, 378 Bacillus idriensis, 225 226 Bacillus insolitus, 363 364 Bacillus licheniformis, 366, 872t Bacillus megaterium, 90 91, 364 Bacillus mucilaginosus, 378 Bacillus pumilus, 363 Bacillus safensis, 863t Bacillus sp., 361, 363 364, 367, 863t, 872t Bacillus subtilis, 225 226, 359 363, 516, 872t Bacillus thuringiensis, 84 85, 365 366 Backcross (BC) 1 (BC1), 917 BAK1 (BRI1 ASSOCIATED RECEPTOR KINASE1), 410 411 Barley, loci for salt stress related ion homeostasis, 940 941 BAZ-hydroxylase, 564 BC inbred line (BIL), 928, 936 937 β-carotene, 400 Beta radiation, 108 Beta vulgaris, 485 486, 650 Bioaugmentation, 218 Biochar, 62 63 Biofilters, 218

Index

Bioremediation, 216 219 ex situ bioremediation, 217 slurry-phase bioremediation, 217 solid-phase bioremediation, 217 in situ bioremediation, 217 engineered in situ bioremediation, 217 intrinsic in situ bioremediation, 217 technologies, 217 219 bioaugmentation, 218 biofilters, 218 bioslurping, 218 biosparging, 218 biostimulation, 218 bioventing, 217 218 composting, 219 land farming, 218 219 Bioslurping, 218 Biosparging, 218 Biostimulation, 218 Biosurfactant production, 371 Biotic stress, 8, 467 468, 543 544 Biotin switch technique (BST), 795 796 Bioventing, 217 218 Biparental cross population, 917 918 BKI1, 411 Boron, 39 Boron deficiency quantitative trait loci, 930 Boron efficiency coefficient (BEC), 930 Boron toxicity, 934 Brachypodium distachyon, 520, 761 Bradyrhizobium, 359, 866 867 Brassicaceae, 222 Brassica chinensis, 632 633 Brassica juncea, 29t, 222, 226, 565t, 744, 758 759, 762 763, 796 797, 840 841 Brassica napus, 12, 293, 473t, 489 490, 500 Brassica oleracea, 143 144, 293, 485 486 Brassica rapa, 763 Brassica species, 763, 801 Brassinolide (BL), 409 410, 410f, 526 527 Brassinosteroids (BRs), 398 399, 409, 411f, 412 413, 513 514, 526 527, 544 546, 545t, 549 550 biosynthesis, 409 410 signaling, 410 413 Breeding, 890 Brevibacillus, 872t BRI1 (BRASSINOSTEROID INSENSITIVE1), 410 412 BRL1, 549 550 BRL3, 549 550 Broccoli (Brassica oleraceavar. italica), 937 Burkholderia, 378, 867 Burkholderia cepacia, 359 361, 363 Burkholderia phytofirmans, 366

971

Burkholderia sp., 863t, 872t BZIP/HD-ZIP-proteins, 827

C Cachlorophyll a/b genes, 305 Cadaverine, 481 482 Cadmium, 182, 209t, 213 214, 226, 272 275, 559, 565t, 698 699 toxicity, 933 934 Caffeoylserotonin, 778 779 Cajanus cajan L., 560 561 Cakile maritima, 13t, 742 Calcineurin B-like proteins, 54 55 Calcium (Ca21) signaling, 2 Calcium, 38 39 Calcium-dependent protein kinase, 256 257 Calcium nitrate, 485 486 Calcium phosphates, 376 377 Caldopentamine, 489 490 Calmodulin (CaM), 513 514 Calmodulin-mediated alterations, 529 CaLRubisco, 305 Calvin Benson Bassham cycle, 682 686 carboxylation, 682 reduction, 682 683 regeneration, 683 Calvin cycle, 244, 264, 328 329 Calvin cycle enzymes, 683 686, 684f carboxylation, 682f fructose-1,6-bisphosphate aldolase, 685 fructose bisphosphatase (FBPase), 683 684 glyceraldehyde-3-phosphate dehydrogenase (GADPH), 685 phosphoglycerate kinase (PGK), 685 phosphoribulokinase (PRK), 684 685 reductions, 683f ribose-5-phosphate isomerase, 686 ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), 683 ribulose-5-phosphate 3-epimerase (RPE), 685 686 sedoheptulose-bisphosphatase (SBPase), 684 transketolase, 685 triose-phosphate isomerase (TPI), 685 Calvin cycle regulation and its enzymes under abiotic stresses, 686 703 heavy metal stress, 695 699 ozone stress, 699 701 salt stress, 691 693 temperature stress, 693 695 high temperature, 693 694 low temperature, 694 695 UV-B stress, 701 703 water stress, 686 691

972 Camalexin (3-thiazole-2’-yl-indole), 341 CaM-binding proteins, 529 CAMTA3, 341 343 CBP60, 341 343 Campestanol, 409 410 Canavalmine, 481 482 Capsicum annuum, 25 26, 29t, 310 311, 336 337, 485 486 N-Carbamoylputrescine, 482 483 N-Carbamoylputrescine amidohydrolase (CPA), 482 483 Carbohydrates, 756 758 fructans, 757 758 raffinose family of oligosaccharides, 757 758 starch, 757 trehalose, 756 757 Carbon dioxide equilibrium, 82 83 Carbon isotope discrimination (CID), 921 Carbonylation, 513 514, 517 518, 522, 524 525, 682 2-Carboxyarabinitol-1-phosphate (CA1P) inhibitor, 689 Cardaminopsis halleri, 672 Carlactone (CL), 434 Carotenoid biosynthesis, 246 247 Carotenoid cleavage dioxygenases (CCDs), 434 Carotenoids, 243, 670 Caryophyllaceae, 222 Casein kinase (CKB3)proteins, 474 Casparian strips, 836 837 Caspase-3-like activities, 8 Caspases, 6 CaSRubisco, 305 Catalase (CAT), 26 27, 243, 323 326, 335, 556 Catharanthus roseus, 590, 871 872 Cation diffusion facilitators (CDFs), 842 Cation diffusion facilitators/metal tolerance proteins, 842 Cation-exchange capacity (CEC), 277 278 CBF1, 814 815 CBF2, 814 815 CBF gene, 814 815 CCA1, 814 815, 817 Cd-poisoned common pepper (Capsicum annuum L.), 336 337 Cd-stressed lupin (Lupinus micranthus Guss.) leaves, 341 343 Cd treatments, 828 Cell membrane stability, 922 923 Cellular defense mechanism, 514 515 Cellular dehydration, 51 52 Cellular organelles, 88 Cellular responses, 88 Cellular transporters, 841 Chaperon proteins, 516

Index

Chelators, 278 Chemical pesticides, 238 Chenopodium botrys, 13 15 Chilling and cold stress genes and transcriptional factors regulation of, 829 Chilling-induced photo-oxidative damage, 38 39 Chilling stress, 565t Chilling stress in plants, 26 32 Chinese cabbage (Brassica campestris L.), 334 335 ChIP-seq analyses, 818 Chlorella saccharophila, 10t 4-Chloroindole-3-acetic acid, 406 Chlorophyll, 186 187 and carotenoid biosynthesis, 246 247 Chloroplastic 13-lipoxygenase (13-LOX), 553 554 Chloroplastic antioxidants, 4 5 Chloroplasts, 328 329 Chlorotic and necrotic areas, 238 Chorismate, 426 Chorispora bungeana, 737 738, 744 Chromate, 272 275 Chromatin immunoprecipitation techniques, 519 520 Chromium, 184 185, 209t, 215, 272 275, 489, 699 toxicity, 935 Chrysanthemum morifolium L., 294 Chryseobacterium, 359 Chrysopogon zizanioides, 763 Cicer arietinum, 29t, 762 763 Cicer arietinum L. cv. Gokce, 336 337 Cinnamic acid (CA), 426 Cinnamoylserotonin, 778 779 Circadian clocks, 811 824 abiotic stress affecting clock genes transcription, 816 817 circadian clock mediating hormone signaling, 817 818 regulating plant response to cold stress, 814 815 regulating plant response to drought stress, 813 regulating plant response to salt stress, 812 813 regulating stress-responsive genes, 815 816 Citrate, 159 Citric acid cycle (CAC), 159 Citrullus lanatus L., 292 Citrus, 473t Citrus aurantium L., 784 785 CKI1, 550 551 Climate change, 78 79, 468 469, 884, 891 892 and sea levels, 892 Clock genes transcription, abiotic stress affecting, 816 817 Clustered regularly interspaced short palindromic repeat (CRISPR)-Cas9, 581 583 Coexpression networks, 592 593

Index

Coincident QTL (cQTL), 917 918 COLDAIR (cold-assisted intronic noncoding RNAs), 472 474 Cold-hardening process, 26 27 Cold-regulated (COR) transcription, 814 Cold stress, 253 254, 489 490, 505 506, 671 672, 937 940 circadian clock regulating plant response to, 814 815 Colloidal fructans, 258 259 COMATOSE (CTS), 425 Common bean (Phaseolus vulgaris), 585 586 Common beech (Fagus sylvatica L.), 338 339 Common sunflower (Helianthus annuus L.), 334 335 Common wheat (T. aestivum L.), 338 339 Composting, 219 Confocal laser scanning microscopy, 796 797 Constitutive triple response1 (CTR1), 414 415 Conventional linkage mapping, 838 839 COOLAIR (cold-induced long antisense intragenic RNAs), 472 474 Copper, 209t, 489, 559 560 toxicity, 840 841, 936 COR15A, 415 416 COR gene, 814 815 Coronatine (COR), 428 Cotton fibers, 613 4-Coumaroylserotonin, 778 779 cPTIO (carboxy-PTIO potassium salt), 341 343 Crambe abyssinica, 745 746 Craterostigma plantagineum, 473t, 649 CRE1/AHK4, 550 551 Creeping bentgrass (Agrostis stolonifera L.), 937 C-repeat binding factor (CBF)-independent transcriptional pathway, 515 516 C-repeat/Drought-responsive element-binding factor dependent (DREB), 515 516 Crisphead lettuce (Lactuca sativaL.), 937 Crop productivity, improvement of, 826 827 CRT/DRE elements, 844 845 CSD1, 475 CSD2, 475 C-terminal inhibitory propeptide, 7 CTR1, 552 553 C-type ATP-binding cassette transporter (OsABCC) family, 841 842 Cucumber (Cucumis sativus L.), 784 785 Cucumis melo, 485 486 Cucumis sativus, 10t, 29t, 515 516, 654 655 Cucumis sativus L, 293, 565t, 784 785 Cucurbita ficifolia, 486 488, 487t, 654 655 Cucurbita maxima, 742 Cultivated tobacco (Nicotiana tabacum L.), 335 336

973

Cunoniaceae, 222 CuO NPs, 869 Cupriavidus metallidurans, 224 225 CUP-SHAPED COTYLEDON genes, 721 722 Cyanidioschyzon merolae, 225 226 Cyanobacteria, 110 111 Cyclic guanosine monophosphate (cGMP), 430 Cyclitols, 759 Cyclobutane pyrimidine dimers (CPDs), 112 113 Cynodon dactylon, 689, 784 785 Cyperaceae, 222 Cyperus eragrostis Lam, 162 163 Cysteine proteases, 7 Cysteine-rich RLKs (CRKs), 5 6 Cytochrome c, 5, 242 Cytokinin (CK), 92 93, 398 399, 420, 422f, 543 544, 545t, 550 551, 557 biosynthesis, 420 421 signaling, 421 423 Cytoplasmic male-sterile mutants (CMSII), 329 330

D Data handling and analysis, 594 Datura stramonium, 487t Daucus carota, 29t DAWDLE assist DCL1, 720 DCL1, 471 472 DCL4, 471 472 dcl mutants, 721 722 DDF2 gene, 304 305 Defective in anther dehiscence1 (DAD1), 424 Dehydration avoidance and tolerance, 86 Dehydration proteins, 516 Dehydration responsive element binding protein (DREB1)/CBF family transcription factors, 527 6-Dehydroteasterone, 409 410 Delayed response genes, 826 Delayed senescence. See Stay-green DELLA proteins, 416, 419, 527, 551 552, 721 722 Δ1-pyrroline, 482 483 6-Deoxocathasterone, 409 410 6-Deoxoteasterone, 409 410 6-Deoxotyphasterol, 409 410 1-Deoxy-D-xylulose-5-phosphate, 400 2-Deoxy glucose (2-DG), 500 6-Deoxy glucose (6-DG), 500 2-Deoxy mannose, 500 Desiccation, 246 Detoxifying enzymes, 826 827 Developmentally regulated programmed cell death (dPCD), 1 2 Diamine oxidases (DAOs), 482 484 1,3-Diaminopropane (DAP), 481 482

974

Index

Dianthus caryophyllus, 486 488, 487t Dianthus stramonium, 487t Dicer, 470 471 Dicer-like (DCL) proteins, 470 471 2,4-Dichlorophenoxy acetic acid (2,4-D), 242 Diffuse radiation, 107 108 Diflufenican, 246 Digalactosyldiacylglycerol (DGDG), 88, 143 Dimethylallyl diphosphate (DMAPP), 421 Dinitrogenase, 865 Diquat act, 241 Direct radiation, 107 108 Diurnal (day/night) variation, 779 DNA methylation, 468 469 DONGLE (DGL), 424 Dorsha, 470 471 Double haploid lines (DHLs), 917 Downstream photoreceptors, inducers of, 828 829 Draught stress, 565t DREB1, 652 DREB1A, 486 488, 650 DREB1B, 486 488 DREB1/CBF, 829 DREB2, 652 DREB2B, 486 488 DREB protein, 828 DRE-specific binding factors, 827 DRIP1 (DREB2A-INTERACTING PROTEIN1), 405 Drosophila melanogaster, 35 36 Drought, 77, 257 258, 617, 745 746, 884 885 causes of, 78 79 exogenous amendments for combating, 89 90 inorganic amendments, 90 organic amendments, 89 90 and flooding-induced programmed cell death, 10 11 genetic engineering of drought-tolerant crops, 94 impacts of, 79 84 metabolic changes, 82 83 physiological changes, 83 84 microbe plant interactions, 90 94 mycorrhizal association, 93 94 plant growth promoting rhizobacteria (PGPR), 91 93 plant mechanism to cope with, 85 89 antioxidant response, 87 88 biochemical responses, 87 cellular responses, 88 dehydration avoidance and tolerance, 86 gene induction and expression, 88 89 growth and physiological modification, 86 metabolic responses, 88 nutrient acquisition habits, 86 87 organelle response, 89

protein synthesis, 87 stress, signaling of, 85 salient features of drought-tolerant plants, 94 soil biota activity, 84 85 soil physicochemical activities, 85 Drought/desiccation stress, aquaporins in, 648 650 Drought escape, 686 687 Drought resistance, 77 78, 686 687 Drought stress, 294, 306 307, 364 367, 918 924 circadian clock regulating plant response to, 813 genes regulation and transcriptional factors, 827 828 hormonal response under drought, 921 microRNA and, 724 osmotic adjustment (OA), 922 plant growth promoting rhizobacteria and alleviation of, 365 367 antioxidative enzymes, induced plant synthesis of, 366 exopolysaccharides (EPS), generation of, 367 osmolytes (compatible solutes) accumulation, 366 367 phytohormonal content, modifications in, 365 366 stress-induced ethylene production, 366 root responses under drought, 922 923 tolerance to, 664 665 water-use and photosynthetic activity under drought, 921 922 yield responses under drought, 923 924 Drought-stressed wheat (Triticum aestivum L.), 337 338 Drought tolerance, 918 920 in pearl millet, 920 921 DSP4 gene, 518 519 Duckweed (Landoltia punctata), 634 635

E E3 ubiquitin ligase, 528 Early response genes, 826 Ectomycorrhizas, 278 Egypt, sugar industry in, 894 897 Eichhornia crassipes (Mart.), 334 335 Eichornia crassipes, 778 EIN2, 552 553, 818 EIN3, 415 416, 552 553 Electron acceptor monodehydroisosorbide (MDHA), 336 337 Electron transport chain (ETC), 628 Eleusine coracana, 139 141 Endogenous hormonal response, 163 168 abscisic acid (ABA), 167 ethylene, 165 166 gibberellins, 163 165 salicylic acid (SA), 167 168 Endoplasmic reticulum (ER), 646

Index

Endoribonuclease, 471 472 Engineered in situ bioremediation, 217 Enhanced suberin1-1 (esb1-1), 836 837 Ent-copalyl diphosphate synthase, 551 Enterobacter, 60, 356, 866 867 Enterobacter aerogenes (LJL-5), 863t Enterobacter cloacae CAL3, 863t Enterobacter cloacae HSNJ4, 863t Enterobacter cloacae ZNP-3, 863t Enterobacter ludwigii PS1, 863t Enterobacter sp., 361, 363 364, 366, 863t Ent-kaurene synthase, 551 Environmentally induced programmed cell death (ePCD), 1 2 Environmental stresses, 481 484, 663 Enzymatic antioxidants, 3 24-epiBL, 526 527, 563 24-Epibrassinolide, 560 561 24-Epibrassinosteroid (24-EBL), 560 561 9-cis-Epoxycarotenoid dioxygenase (NCED), 167, 305, 527 528 Eragrostis nindensis, 649 ERD10B, 652 ERD10C, 652 ERD genes, 652 Eruca sativa L., 307 Escherichia coli, 224 226 Ethanol production, 829 830 Ethylene (ET), 28, 56, 92, 165 166, 281 282, 341 343, 356, 398 399, 413, 414f, 438 439, 543 544, 545t, 552 553, 557, 785 biosynthesis, 413 production, 874 signaling, 413 416 Ethylene response factors (ERFs), 160, 168 169 Ethyl methanesulfonate (EMS) mutagenesis, 63 64 ET-responsive element-binding factors (ERFs), 413 Eucalyptus, 649 650 Eucalyptus camaldulensis, 56 Eucalyptus globulus, 654 655 Euphorbiaceae, 222 Exiguobacterium oxidotolerans, 363 Exogenous amendments for combating drought, 89 90 inorganic amendments, 90 organic amendments, 89 90 Exopolymers, production of, 372 Exopolysaccharides (EPS), 362 364 generation of, 367 production of, 363 364 Ex situ bioremediation, 217 slurry-phase bioremediation, 217 solid-phase bioremediation, 217

F Fabaceae, 222 Fagus sylvatica L., 338 339 Fasciclin domains, 254 Fatty acids (FAs), 330 331, 430 FBH3 (FLOWERING BHLH3), 404 Fenton reaction, 840 Ferredoxin, 328 329 Ferritin protein, 690 691 Fertilizers, 890 891 Feruloylserotonin, 778 779 Flacourtiaceae, 222 Flavin groups, 330 331 Flavobacterium, 359 Flavonoids, 113 114, 296, 323 326, 666 Flavoprotein AtHAL3, 826 827 FLC gene, 472 474 Flood(ing), defined, 157 159 Flooding, 11, 690 691, 887 888 Flooding-induced programmed cell death, 10 11 Flooding stress, 157 159 plants strategies against, 159 162 escape strategy under submergence, 159 160 quiescence strategy under submergence, 160 water logging tolerance strategy, 160 162 transcriptional factors regulation of, 830 Flooding tolerance mechanisms, 162 169 endogenous hormonal response, 163 168 abscisic acid (ABA), 167 ethylene, 165 166 gibberellins, 163 165 salicylic acid (SA), 167 168 genetic response, 168 169 morphological response, 162 163 Flooding/waterlogging/submergence tolerance, 942 943 Flowering, 499 Flower patterning protein, 828 Fluorescence transient (FT) analysis, 700 701 Flurochloridone, 246 Flurtamone, 246 Foeniculum vulgare, 758 Forage crop breeding, 924 Frost tolerance QTL, 939 Fructans, 505 506, 757 758 Fructose, 498, 505 506 Fructose-1,6-bisphosphatase, 689 690 Fructose-1,6-bisphosphate aldolase, 685 Fructose-2,6-bisphosphate, 264 Fructose bisphosphatase (FBPase), 683 684 FullsibF1 (pseudo-testcross), 917 Fungal plant interaction, 61 62

975

976

Index

Fungal plant interaction (Continued) arbuscular mycorrhizae (AM) in salt-affected soils, 61 arbuscular mycorrhizae plant association on plant growth, 61 62 Fusarium oxysporum, 53 Future of sugar beet industry (FOSI), 912 916 in North Egypt, 897 899 structure model of, 912, 912f

G GALACTOLIPASE A1 (GLA1), 424 Galactose, 499, 758 L-Galactose-γ-lactone dehydrogenase (GLDH), 330 Gametophytes, 612 γ-aminobutyric acid, 482 483 γ-amino-N-butyric acid (GABA), 758 759 γ-glutamylcysteine synthetase, 523 524 Gamma radiation, 108 109 Garden tomato (Lycopersicum esculentum Mill.), 334 335 G-box binding, 828 829 Gene Expression Omnibus, 583 584 Gene induction and expression, 88 89 Gene regulation and transcriptional factors in plant response to drought stress, 827 828 in plant response to salt stress, 826 827 Gene regulatory networks, 592 Genetically engineered plants, 826 827 Genetically modified organism, 223 Genetic mapping approaches, 835 836 Gene-to-metabolite networks, 590 Genevestigator, 583 584 Genipa americana, 14t Genomics, 581 583 Genotyping-by-sequencing (GBS), 918 20-C Geranylgeranyl diphosphate (GGDP) precursors, 417 418 Germination, 28 GGPP (trans-geranylgeranyl diphosphate), 551 Gibberellic acid (GA), 281 282, 502, 545t, 551 552, 557 Gibberellin (GA), 159 160, 163 165, 398 399, 416 419, 513 514, 527, 543 544 biosynthesis, 417 418 signaling, 418 419 GID1, 551 552 GIGANTEA (GI), 812 813 Global agriculture, impact on, 81 84 individual plant, impacts on, 81 84 metabolic changes, 82 83 physiological changes, 83 84 Global weather alteration, 885 Glomus etunicatum, 61 62

Glomus intraradices, 131 132, 139 141 Glomus versiforme, 139 141 GlpF-like intrinsic proteins, 644 646 Glucans, 258 259 Glucose, 498, 505 507 Glucose-6-phosphate (G-6-P), 500 3-Glutamyl cysteine dipeptidyl transpeptidase, 280 Glutaredoxin (GRX), 340, 429 Glutathione (GSH), 243, 323 326, 557, 741 742 Glutathione peroxidase, 826 827 Glutathione reductase, 485 486 Glutathione S-transferase (GST), 26 27 Glutathionylation, 513 514, 517 518, 522 524 Glyceraldehyde-3-phosphate dehydrogenase (GADPH), 685 Glyceraldehydes-3-phosphate, 400 Glycerol-facilitator AQPs (GLPs), 644 646 Glycine betaine (GB), 759 760, 843 844 Glycine max, 29t, 35 36, 124 125, 163, 164f, 473t, 565t, 644, 868 869 Glycine-rich RNA-binding protein 7 (GRP7), 813 Glycine soja, 651 Glycophytes, 51 52, 54 Glycosylations, 513 514, 519 Gold NPs (nAu), 631 Gonyaulax polyedra, 775 776 Gossypium barbadense, 29t Gossypium hirsutum, 9 Gossypium tomentosum, 941 942 GPX gene, 335 336 Grain crops, 924 Greenhouse gas (GHG), 78 79, 105 107, 885, 889 elevation of, 886 Growth attributes, by plant growth-promoting rhizobacteria, 862 Growth attributes of plants affected by water deficit, 185 186 Growth-regulating factor 7 (GRF7), 405 GRP3A and PRS9, 872t Grp7 mutant, 813 GSH reductase (GR), 336 337 GSH γ-glutamylcysteinyl transferase. See Phytochelatin synthase (PCS) Guaiacol peroxidase, 485 486 Guard cells, 612 613

H H2O2, 825 826 H3K4me3, 520 521 H3K9ac, 520 521 H3K9me2, 520 521 H3K23ac, 520 521 H3K27ac, 520 521

Index

H3K27me3, 520 521 H4ac, 520 521 Haber Weiss reaction, 34 35, 178 179 Halomonas variabilis, 363 364 Halophytes, 54, 57 58, 60 61 Halotolerant microbe mediated processes, 60 61 Halotolerant plants, genetic engineering of, 63 64 Heat-shock domain, 35 36 Heat-shock elements (HSEs), 35 36 Heat-shock factors (HSFs), 35 36 Heat-shock proteins (HSPs), 26 27, 35 36, 87, 281, 306, 780, 847 Heat stress, 28, 252 253, 489 490, 669 671, 743 744, 780 781, 936 937 Heat stress, plant adaptations to, 33 39 biochemical adaptation, 34 35 molecular adaptation, 35 36 nutrient management approach, 36 39 role of macronutrients, 37 39 role of micronutrients, 39 physiological adaptation, 33 34 Heavy metal (HM), 207 208, 744 745, 798 799, 871 effect on plants, 839 840 ionomics of, 841 842 cation diffusion facilitators/metal tolerance proteins, 842 natural resistance-associated macrophage protein transporters, 842 P1B-ATPases/heavy metal ATPases, 841 842 ZRT, IRT-like proteins transporters, 842 843 and nanoparticle-induced programmed cell death, 13 16 stress response in plants, 843f toxicity, 840 841 mechanism of, 841 843 Heavy metal (HM) stress and plant life, 271 288 avoidance mechanisms, 278 279 consequences of heavy metals in plants, 276 heavy metals detoxification/tolerance in plants, 278 heavy metals uptake and transport in plants, 277 278 metal binding to cell wall, 279 280 metal bioavailability, sources and, 275 276 tolerance mechanisms, 280 282 Heavy-metal effects on plants, 176 185 cobalt, 181 copper, 176 essential heavy-metal elements, 176 182 cobalt, 181 copper, 176 iron, 177 179 manganese, 179 180 molybdenum, 181 182

977

nickel, 180 181 zinc, 177 iron, 177 179 manganese, 179 180 molybdenum, 181 182 nickel, 180 181 toxic heavy metals, 182 185 cadmium, 182 chromium, 184 185 lead, 182 183 mercury, 183 184 zinc, 177 Heavy metal stress, 559 561, 672 673, 695 699 and its transcriptional factors regulation, 828 829 microRNA and, 723 Heavy metal toxicity stress, 367 373 plant growth promoting rhizobacteria and alleviation of, 368 373 1-aminocyclopropane-1-carboxylate deaminase, synthesizing, 370 biosurfactant production, 371 exopolymers, production of, 372 heavy metals, diminished uptake of, 372 373 heavy metals resistant genes induction, 373 380 micro- and macronutrients, betterment in the uptake of, 372 organic acids, production of, 371 phosphate solubilization, 370 phytohormones, generation of, 371 siderophores, generation of, 368 370 Helianthus annuus, 56, 565t, 784 785 hen1 mutant, 721 722 Herbicide-induced modification, 242 Herbicides, 237 250 chlorophyll and carotenoid biosynthesis, 246 247 list of natural products used as, 239t phenotypical manifestation, 238 physiological damage through generated ROS intermediates, 241 244 antioxidant defense in response to herbicide treatment, 243 244 lipid peroxidation, 242 243 protein oxidation, 242 physiological process, direct damage to, 244 246 amino acid biosynthesis, 245 246 photosystem II inhibitor, 245 photosystem I inhibitors, 245 Heteropolysaccharides, 258 259 Hexadecatrienoic acid, 553 554 Hexokinase (HXK) dependent sugar signaling pathway, 500 Hexokinase (HXK) independent sugar signaling pathway, 500

978

Index

Hexose sensing, 500 High-affinity potassium transporter (HAK5), 837 838 High and low temperature induced programmed cell death, 9 High-density genetic maps, 918 High molecular mass polysaccharides (HMMC), 258 260 High-temperature (HT) stress, 743 744 High temperature induced PCD, 9 High-temperature stress, 9 Histidine kinase (HK), 399 Histone, 520 521, 521f Histone acetyltransferase (HAT), 513 514 Histone deacetylase (HDAC), 513 514 HKT1 gene, 356 357 HKT-type Na1 transporters, 846 HLS1, 415 416 Homeostasis, 59 28-Homobrassinolide, 526 527, 560 561 Homo sapiens, 487t Homospermidine, 481 482 Hordeum maritimum, 764 Hordeum spontaneum, 689 690 Hordeum vulgare, 29t, 56, 293 294, 473t, 489, 649 650, 724, 764 Hormonal response under drought, 921 Hormone, sRNAs in signaling of, 476 Hormone-mediated stress tolerance, in plants, 526 528 abscisic acid, 527 528 auxin, 526 brassinosteroids, 526 527 gibberellins, 527 Hormone regulation, 55 57 hormonal-modified proline metabolism and plant growth, 55 57 abscisic acid, 56 ethylene, 56 nitric oxide, 57 salicylic acid, 56 Hormones, 141 142 Hormone signaling, circadian clock mediating, 817 818 HPS101, 490 HPS70, 490 HPS90, 490 HXK1, 500 501 HXK2, 500 501 Hybrid intrinsic protein, 644 646 Hydrogen cyanide (HCN), 356 Hydrogen peroxide, 3 13-Hydroperoxy derivative of linolenic acid (13HPOT), 553 554 Hydroxycinematics, 666

2-Hydroxymelatonin, 778 P-Hydroxyphenylpyruvate dioxygenase (HPPD), 246 247 5-Hydroxytryptamine, 775 hyl1 mutant, 721 722 Hyperaccumulation, 281 Hyperaccumulators, 222 Hypericum perforatum, 672 Hypericum retusum, 667 Hypersensitive to phosphate starvation 1 (hps1) mutants, 142 Hypertrophy, 163 Hypocotyl growth, 500 HYPONASTIC LEAVES1 (HYL1), 720

I IAA (indole-3-acetic acid), 371, 406, 407f IBA (indole-3-butyric acid), 406 Ice plants (Mesembryanthemum crystallinum L.), 335 336 Imazamox, 242 Imidazolinones, 245 246 Indica, 934 Indolamines, plant stress physiology and role of, 779 786 biological stress, 785 786 chemical stress, 783 785 heavy metal stress, 783 784 salinity stress, 784 785 environmental stresses, 779 782 temperature stress, 779 781 UV stress, 782 water stress, 781 782 Indole-3-acetamide (IAM) pathway, 869 Indole-3-acetic acid (IAA), 543 544, 545t, 560 Indole-3-acetic aldehyde (IAA), 861 862, 866 production, 866 867 Indole-3-acetonitrile (IAN), 866 867 Indole acetic acid (IAA), 60, 90 92 IAA8, 305 Induced systemic resistance (ISR), 364, 867 868, 870 871 Induced systemic tolerance (IST), 364, 871 872 Industrial effluents, 209 210 Inorganic ions, 54 Inorganic phosphate (Pi), 123 Inositol hexakisphosphate, 376 377 Inositol polyphosphate 1-phosphatase (IPPase), 683 684 Inositol pyrophosphates (PP-InsPs), 142 143 In situ bioremediation, 217 engineered in situ bioremediation, 217 intrinsic in situ bioremediation, 217 Interactomics, 586 587

Index

Intercellular signaling, 54 55 Intracellular ROS, 827 Intrinsic in situ bioremediation, 217 Introgression lines (IL), 919 920 Iodosulfuron, 242 Ion-channel leading, 399 Ion homeostasis in plants, 362 363 Ionic homeostasis, nanoparticles application and, 632 633 Ionizing radiation, 107 108 Ionomics in plant abiotic stress tolerance, 835 860 effect of heavy metal on plants, 839 840 forward genetics and ionomic gene identification, 836 839 heavy metals, ionomics of, 841 842 cation diffusion facilitators/metal tolerance proteins, 842 natural resistance-associated macrophage protein transporters, 842 P1B-ATPases/heavy metal ATPases, 841 842 ZRT, IRT-like proteins transporters, 842 843 heavy metal toxicity, 840 841 mechanism of, 841 843 osmolytes in plant protection, 843 845 late-embryogenesis-abundant- type proteins in salt stress, 844 845 osmotic stress effect on plants, 846 847 ionomics of, 847 849 salt stress, ionomics of, 845 846 HKT-type Na1 transporters, 846 V-type H1 ATPases, 846 salt stress and plants, 843 Iositol-1-phosphatase (IMPase), 683 684 Ipomoea batatas, 29t, 486 488, 487t, 742 Iron, 272 275, 866 Iron deficiency quantitative trait loci, 929 930 Iron toxicity, 934 935 IRT-like proteins transporters, 842 843 Isopentenyl pyrophosphate (IPP), 400 Isoproturon, 242

J Japonica, 934 Jasmonates (JAs), 118 119, 553, 557 Jasmonic acid (JA), 281 282, 398 399, 423 424, 425f, 543 546, 545t, 553 554, 785 biosynthesis, 424 425 signaling, 426 428 Jatropha curcas L., 689 Jatropha integerrima, 293

979

K Karrikins (KARs), 398 399, 436, 436f signaling, 437 3-Ketoacyl-CoA thiolase (KAT2), 553 554 Klebsiella, 866 867 Klebsiella pneumonia, 863t Kluyvera ascorbate, 872t K-mediated ATPase, 28 32 K-solubilizing bacteria (KSB), 377 378

L Laccase-like proteins (LAC), 474 Lactuca sativa, 485 486, 635 Lamiaceae, 222 Land farming, 218 219 Landoltia punctata, 634 635 Late-embryogenesis-abundant (LEA) gene, 515 516, 581 583 Lateral root growth, mechanism of changes in, 126 Lavandula plants, 84 85 Lead, 182 183, 209t, 212, 227, 698 Leaf and leaf size and morphology, sRNAs in the development of, 474 Leaf orientation, 33 34 Lea genes, 827 828 LEA proteins, 516 Legumains, 7 Legumes, cold tolerance in, 939 Leifsonia xyli SE134, 863t Lemna minor, 108, 630 Lettuce (Lactuca sativa), 635 Lettuce plant seeds, 33 34 Leucine-rich repeat (LRR), 410 Leuconostoc mesenteroides, 253 254 Leymus chinensis, 692 Lhcb, 112 113 LHY, 814 815 Life, source of on earth, 107 Light-induced Taiwan alder [Alnus formosana (Burkill) Makino], 336 337 Light metals, 207 208 Light stress and UV in medicinal plants, resistance to, 665 668 Light uptake by plants, consequences of, 828 829 Lipid metabolism, 563 Lipid peroxidation, 242 243 Lipids, 143 Lipoamide dehydrogenase (LPD), 697 698 Lipoxygenase (LOX), 425 Liquid silver. See Mercury Lolium multiflorum, 279 Lolium perenne, 191 192, 293, 634 635

980 Lotus japonicas, 132 133 Lotus japonicus, 868 869 Lotus tenuis, 162 163 Low N (LN), 925 926 LOW PHOSPHATE ROOT1 (LPR1), 125 LOW PHOSPHATE ROOT2 (LPR2), 125 Low-temperature (LT) stress, 744 Low temperature stress, aquaporins in, 651 652 LOX2, 553 554 LOX3, 553 554 LOX4, 553 554 Luffa cylindrica, 565t Lupinus albus, 785 786 Lupinus luteus, 740 741 Lupinus micranthus Guss., 341 343 LUX, 816 817 LUX promoter, 817 Lycium barbarum, 764 Lycium ruthenicum, 759 760, 764 Lycopersicon esculentum, 15t, 485 486 Lycopersicon pennellii IL, 941 942 Lycopersicum esculentum Mill., 334 335 Lysigenous aerenchyma, 11

M Macro-minerals, quantitative trait loci (QTLs)related to, 925 929 Macronutrients, role of, 37 39 Macrotyloma uniflorum, 758 Magnesium, 39 Maize (Zea mays subsp.), 338 339 Major facilitator superfamily (MFS), 128 Malondialdehyde (MDA), 93, 242 243 Malondialdehyde, 506 507 Maltose, 499 Malus baccata, 781 Malus domestica, 487t Malus hupehensis, 784 785 Malus zumi, 651 Manganese, 39 toxicity, 935 Manganese deficiency quantitative trait loci, 930 Mannitol, 759 MAPK, 412, 440 441, 558 MAPK2 gene, 304 305 MAPK kinase kinase (MAPKKK) YDA, 412 MAPKKKs, 552 553 MAPK pathway, 518 519 Marker-assisted BC (MABC), 920 921 Marker-assisted selection (MAS), 917 Mass spectrometry, 519 520 Matricaria necati, 665 MDHAR (monodehydroascorbate reductase), 336 337

Index

Medicago falcata, 652 Medicago sativa, 37 38, 635, 868 869 Medicago species, 764 Medicago truncatula, 128, 131 132, 473t, 760 761, 937 Medicinal and aromatic plants, resistance mechanism of to temperature stress, 668 669 Medicinal plants, resistance to light stress and UV in, 665 668 Mehler reaction, 328 329 Meiosis, 470 MEKK1 protein, 340 341 Melatonin, 761, 762t, 775, 778 779, 781 782, 785 786 biosynthesis of, 776 778 Melilotus siculus, 167 Mentha arvensis, 668 Mentha piperita L., 310 Mercury, 183 184, 209t, 212 213, 224 225, 565t, 698 merR gene, 224 225, 227 Mesembryanthemum crystallinum, 53, 335 336, 649 650 Metabolism, plant, 88 Metabolites’ role in abiotic-stress tolerance, 755 774 abiotic-stress tolerance, 755 future prospects, 763 765 primary metabolites and osmoprotectants, 755 762 amino acids, 758 759 carbohydrates, 756 758 glycine betaine (GB), 759 760 melatonin, 761, 762t polyamines, 760 761 serotonin, 761 762 sugar alcohols (polyols), 759 secondary metabolites, role of, 762 763 Metabolomics, 585 586 Metacaspases, 6 7 Met adenosyl transferase-1, 341 343 Metal and water-deficit stress, combination of, 188 192 on plant growth and physiological processes, 189 190 plant water relations under metal stress, 191 192 Metal bioavailability, sources and, 275 276 Metal-contaminated sites, 215 216, 227 Metallic elements, 207 210 Metalloids, 207 208 Metallothioneins (MTs), 276 Metals, 207 208 occurrence, speciation, and toxic effects, 210 215 arsenic, 214 215 cadmium, 213 214 chromium, 215 lead, 212 mercury, 212 213

Index

phytotoxicity, 276 remediation of toxic metals and metalloids, 215 216 sources of, 209 210 toxicity, 271 272, 278 Metal stress, 489 Methoxyphenone, 246 Methylation, 513 514 Methylerythritol 4-phosphate (MEP) pathway, 701 Methyl jasmonate (MeJA), 553, 557 Methylmercury, 212 213 Methylobacterium oryzae, 872t Metsulfuron, 242 MfPIP2-7, 652 Micro- and macronutrients, betterment in the uptake of, 372 Microbacterium spp., 363 364 Microbe plant interaction, 59 62, 90 94 fungal plant interaction, 61 62 arbuscular mycorrhizae (AM) in salt-affected soils, 61 impact of arbuscular mycorrhizae plant association on plant growth, 61 62 halotolerant microbe mediated processes, 60 61 mycorrhizal association, 93 94 plant growth promoting rhizobacteria (PGPR), 91 93 drought tolerance gene induction in plants, 93 osmolytes accumulation in plant tissue, 93 phytohormone production, 92 root growth modification, 92 93 plant growth-promoting rhizobacteria, 59 60 hormone production for enhanced growth, 60 Microbes, 219 Microbial root colonization, 355 356 Microelectrode ion flux estimation (MIFE), 615 619 aluminum stress, 617 619 salt stress, 616 617 water deficit and oxygen deprivation, 617 Microelements (trace minerals), 379 380 Micro-nutrients quantitative trait loci (QTLs) related to, 929 931 role of, 39 MicroRNAs (miRNAs), 123 124, 137 139, 254, 467 469, 719 734, 726f, 727f biogenesis of, 720 721 and drought stress, 724 future outlook, 726 728 and heavy-metal stress, 723 and oxidative stress, 723 724 in plant growth and development, 721 722 and salt stress, 724 725 and temperature stress, 725 726 upregulation and downregulation of, 728t

981

and UV-B radiation, 725 in various abiotic stresses, 722 723 Microspore abortion, 11 Mid molecular mass polysaccharides (MMMC), 258 260 Mineral nutritional imbalance stress, 373 380 plant growth promoting rhizobacteria and availability of nutrients, 374 380 microelements (trace minerals), 379 380 nitrogen, 374 376 phosphorus, 376 377 potassium, 377 379 Mineral stress, 924 931 QTL related to macro-minerals, 925 929 nitrogen deficiency quantitative trait loci, 925 926 phosphorus deficiency quantitative trait loci, 926 928 potassium deficiency quantitative trait loci, 928 929 QTL related to micro-nutrients, 929 931 boron deficiency quantitative trait loci, 930 iron (Fe) deficiency quantitative trait loci, 929 930 manganese deficiency quantitative trait loci, 930 zinc deficiency quantitative trait loci, 931 Mineral toxicity, 931 936 aluminum, 931 933 boron, 934 cadmium, 933 934 chromium, 935 copper, 936 iron, 934 935 manganese, 935 selenium, 934 zinc, 936 MIR156i, 725 726 MIR167h, 725 726 MiR169, 474 MiR169g, 474 MiR169n, 474 MiR319c, 471 MiR389a, 471 MiR393, 471, 473t, 476 MIR393a, 725 726 MiR395, 471 MIR396e, 725 726 MIR396g, 725 726 MiR397b, 471 MIR398a, 475 MIR398b, 475 MIR398c, 475 miR399f, 135 136 MiR402, 471 miRDeep algorithm, 138 139

982 MiRNA165/166, 474 Mitochondria, 88, 329 330 Mitochondrial permeability transition pores (MPTP), 5 Mitochondrial respiration, 701 Mitogen-activated protein kinase (MAPK), 5, 340 341, 516 Mitogen-activated protein kinase3 (MAPKKK), 415 Mitogen-activated protein kinase4 (MPK4), 426 428 Mitosis, 470 Modulated fluorescence (MF) analysis, 700 701 Molecular phytohormones, 398 399 Molybdenum cofactor sulfurase(MCSU), 527 528 Monocotyledonous flowering plants, 162 163 Monodehydroascorbate reductase (MDAR) enzymes, 741 742 Monogalactosyldiacylglycerol (MGDG), 88, 143 Moringa peregrina, 299 Mo transporter 1 (MOT1) variance, 838 839 Mucuna pruriens (L.) DC, 775 776 Multidrug and toxic compound extrusion (MATE) family transporters, 144 Multienvironment trials (METs), 890 Multiple “omics” data, integration of, 587 589 metabolomic proteomic, 588 589 transcriptomic metabolomic, 588 transcriptomic proteomic, 587 588 Musa acuminata, 29t Musa paradisiaca L., 334 335 Mus musculus, 487t Myb36-1 mutant, 836 837 MYB proteins, 827 Mycorrhizal association, 93 94 Mycorrhizal fungi (MF), 82 83, 358 Mycosporine amino acids (MAAs), 114 116 Myo-inositol, 759

N Nakr1-1 mutant, 837 838 Nanoparticle application, 627 642 and ionic homeostasis, 632 633 and its role in redox regulation, 628 630 nanoparticles toxicity in plants, 633 636 and oxidative stress tolerance, 628 and photosynthetic apparatus, 630 632 uptake, transportation, and translocation of nanoparticles, 627 628 Nanoparticles, 289 322 for abiotic stress management, 301t agronomical aspects of crops, positive effects of nanoparticles on, 308 311 antioxidant compounds induction by nanoparticles, 294 304 antioxidant capacity, 295 296

Index

induction of antioxidant capacity by nanoparticles, 297 300 induction of tolerance to abiotic stress, 300 304 oxidative stress, 294 295 oxidative stress induced by nanoparticles, 296 297 morphological, anatomical, and histological changes induced by, 291 294 nanotechnology and, 290 291 proteomic modifications of plants exposed to nanoparticles, 307 308 transcriptomic modifications by nanoparticles and abiotic stress, 304 307 Nanoparticles stress impact of, over rhizobacteria, 869 Nanotechnology and nanoparticles, 290 291 Nasturtium, 667 Natural attenuation. See Intrinsic in situ bioremediation Natural resistance-associated macrophage protein (NRAMP) transporters, 842 Natural resources and ionomic alleles identification, 838 839 Near-isogenic lines (NILs), 917 9-cis-Neoxanthin, 401 Nickel, 209t, 489, 559 560 Nicotiana attenuata, 424 Nicotiana benthamiana, 473t Nicotiana plumbaginifolia L., 332 333 Nicotiana rustica, 759 760 Nicotiana tabacum, 10t, 12 15, 13t, 14t, 25 26, 29t, 37 38, 224 225, 298, 471, 485 486, 487t, 649 650 Nicotinamide adenine dinucleotide (NADH), 159 Nicotinamide adenine dinucleotide phosphate (NADPH), 682 683 NADPH-dependent-oxidases (NOXs), 323 326, 332 333 NADPH oxidase, 847 849 Nicotinamide adenine dinucleotide phosphatemalic enzyme, 689 690 NIP genes, 652 Nitrate-by-nitrate reductase (NR), 431 Nitrated fatty acids, 802 protein nitroalkylation, 802 Nitric oxide (NO), 57, 398 399, 429 430, 430f, 432f, 793 795, 802 biosynthesis, 430 431 and ozone stress, 746 747 signaling, 431 433 Nitric oxide dependent posttranslational modification of proteins under abiotic stress, 795 802 nitrated fatty acids, 802

Index

protein nitroalkylation, 802 protein S-nitrosylation under adverse environmental stress conditions, 795 799 extreme temperatures, 796 797 heavy metals, 798 799 ozone, 799 salinity, 798 wounding, 797 protein tyrosine nitration during abiotic stress situations, 799 801 extreme temperatures, 800 heavy metals, 801 salinity, 801 wounding, 801 Nitric oxide signaling under abiotic stress, 739 747 drought, 745 746 heat stress, 743 744 heavy metals, 744 745 low temperature (LT), 744 nitric oxide and ozone stress, 746 747 nitric oxide as a long-distance signal during wounding stress, 742 salinity, 740 742 Nitric oxide sources under abiotic stress, 736 739 oxidative pathway, 737 738 nitric oxide like synthase, 737 738 polyamines, 738 reductive pathway, 738 739 nitrate reductase, 739 nonenzymatic, 738 reductive pathways, 739 Nitroalkylation, 794 795 Nitrogen, 55, 86 87, 374 376 Nitrogenase (nif) genes, 865 Nitrogen deficiency quantitative trait loci, 925 926 Nitrogen fixation, 865 Nitrogen fixing rhizobia, 358 NITROGEN LIMITATION ADAPTATION (NLA) mRNA, 138 139 Nitrogen nutrition index, 926 Nitrogen use efficiency (NUE), 925 926 Nitrosoproteome, 796 Nitrosylation, 513 514, 525 NOD26-like intrinsic proteins (NIPs), 644 646 Nonenzymatic antioxidants, 3, 26 27 NONEXPRESSOR OF PR GENES1 (NPR1), 558 Nonionizing radiation, 107 108 Norflurazon, 246 Norin-PL8, 937 938 Norspermidine, 489 490 Norspermine, 489 490 NPR1 (nonexpresser of pathogenesis-related1), 429 NPR1, 554 555

983

NPR3, 554 555 NPR4, 554 555 NtER1 gene, 415 416 N-terminal signal peptide, 7 Nuclear cap-binding complex, 720 Nucleic acids, 376 377, 430 Nutrient acquisition habits, 86 87 Nutrient management approach, 36 39 macronutrients, role of, 37 39 micronutrients, role of, 39 Nutrition-related stresses, 254 255

O Ochrobactrum sp., 872t Ocimum basilicum L., 293 Oligosaccharides, raffinose family of, 757 758 112:50, 836 837 OPDA (cis-12-oxo-phytodienoic acid), 425 Optimal solutions, 899 904 Organelle proteins, overexpression of, 529 530 Organelle response, 89 Organic acids (OAs), 143 144, 275 277 production of, 371 Oryza meridionalis, 693 694 Ornithine decarboxylase (ODC), 482, 487t Oropetium thomaeum, 756 Oryza nivara, 168 169 Oryza officinalis, 937 Oryza rufipogon, 168 169 Oryza sativa, 11t, 13t, 29t, 114, 163 165, 292, 473t, 487t, 581 583, 723 724, 759 760, 784 785 Oryza sativa drought-induced SINA protein 1 (OsDIS1), 528 OsABCC1, 842 843 OsGSR1, 438 OsIRE1, 583 584 Osmolytes, 54, 93 accumulation of, 362, 366 367 in plant tissue, 93 in plant protection, 843 845 late-embryogenesis-abundant- type proteins in salt stress, 844 845 Osmolytic-regulated genes and ion transporters, 827 Osmoprotectants, 33 34, 54 Osmotic adjustment (OA) and accumulation of solutes tolerant to dehydration, 187 188 in plant cell, 58 under drought, 922 Osmotic deregulations, 51 52 Osmotic effect, 12 Osmotic regulations, 54 Osmotic stress, 489 490

984 Osmotic stress (Continued) effect on plants, 846 847 ionomics of, 847 849, 848f Osmotic stress regulated (OR) genes, 847 OsNek6, 521 522 OsWRKY30, overexpression of, 581 583 Oxalate oxidase (OxOx), 331 332 Oxidative modification, 54 Oxidative stress, 109 110, 210, 294 295 microRNA and, 723 724 Oxidative stress biomarkers, generation of, 34 35 Oxidative stress induced by nanoparticles, 296 297 Oxidative stress regulation, sRNAs in, 475 Oxidative stress tolerance, nanoparticle application and, 628 Oxyfluorfen, 241 242 Oxygen-free radicals, 840 Ozone, 799 Ozone stress, 699 701

P P1B-ATPases, 841 842 P5CS2, 415 416 P5CS gene, 304 305 PAA (phenylacetic acid), 406 P-acquisition efficiency (PAE), 124 Paenibacillus polymyxa, 362 Paenibacillus sp., 378, 872t Paeonia lactiflora Pall, 294 PAMP-triggered immunity (PTI), 785 Panax ginseng, 650 Pantoea agglomerans, 364, 367 Pantoea dispersa, 361 362 Pantoea sp., 863t PA oxidase (PAO), 483 484 Papaya, 515 516 Parameters of chlorophyll fluorescence kinetics (PCFKs), 936 937 Paraquat, 241 Paspalum dilatatum, 689 Passiflora incarnata, 29t Pathogen, small interfering RNAs in defense against, 471 472 Pathogen-associated molecular patterns (PAMPs), 785 Pathogenesis-related protein 1 (PR1), 426 428 Pattern-recognition receptors (PRRs), 785 PAZ domain, 471 Pdc1, 829 830 Peanut (Arachis hypogea) yield responses under drought, 924 Peanut cultivar (Arachis hypogaea var. JL-24), 334 335 Penicillium spp., 785 786 Penoxsulam, 242

Index

Pepper (Capsicum annuum), 25 26 Perennial ryegrass (Lolium perenne L.), 634 635 Permease in chloroplasts 1 (PIC1), 695 696 Peroxidase (POD), 26 27, 323 326, 666 Peroxisome, 330 331, 425 Peroxoporins, 4 5 Petunia hybrida, 473t PGPR (plant growth promoting rhizobacteria), 356 361, 380, 873 874 mode of action for, 862 865 PHABULOSA (PHB) Phaseolus vulgaris, 29t, 124 125, 294, 489, 585 586, 689 690, 696 697, 840 841, 868 869 PHA-VOLUTA (PHV) Phellogen, 167 Phenolics, 110, 243, 553 554 Phenols, 785 Phenylalanine ammonia-increase lyase (PAL), 664 665 PHOSPHATE1, 135 PHOSPHATE3 (PHO3), 142 PHOSPHATE DEFICIENCY RESPONSE2 (PDR2), 125 126 PHOSPHATE OVER ACCUMULATOR2 (PHO2) transcript, 137 138 Phosphate solubilization, 370, 865 866 Phosphate-solubilizing bacteria (PSB), 370, 376 377, 865 866 PHOSPHATE STARVATION RESPONSE1 (PHR1), 135 136 Phosphate stress, low, 123 biochemical responses to, 141 145 hormones, 141 142 inositol pyrophosphates (PP-InsPs), 142 143 lipids, 143 organic acids (OAs), 143 144 release of acid phosphatases, 144 145 sugars, 142 changes, mechanism of in lateral root growth, 126 in primary root growth, 125 in root hairs, 126 future prospects, 145 molecular responses to, 126 139 microRNAs, 137 139 PHOSPHATE1, 135 phosphate transporter1 (PHT1), 127 131, 129t, 140t phosphate transporter2 (PHT2), 131 132 phosphate transporter3 (PHT3), 132 133 phosphate transporter4 (PHT4), 133 134 phosphate transporter5 (PHT5), 134 transcription factors (TFs), 135 136, 137t

Index

role of arbuscular mycorrhizae fungal in low phosphate stress tolerance, 139 141 root system architecture, changes in, 124 125 PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1, 128 Phosphatidylcholines, 88 Phosphatidylglycerol, 143 Phosphoenolpyruvate (PEP) carboxylase, 689 690 Phosphofructokinase, 28 32 Phosphofructokinase 2, 264 Phosphoglycerate kinase (PGK), 685 Phospholipase, 529 530 Phospholipase D, 256 257 Phospholipids, 376 377 Phosphoribulokinase (PRK), 684 685 Phosphorous, 123 Phosphorus, 376 377 Phosphorus deficiency quantitative trait loci, 926 928 PHOSPHORUS STARVATION TOLERANCE1, 126 PHOSPHORUS UPTAKE 1, 126 Phosphorus uptake efficiency (PupE), 927 928 Phosphorus use efficiency (PUE), 926 927 Phosphorylation-mediated signal transduction, 5 Phosphorylations, 513 514, 518 519 Photobleaching, 246 Photolyases, 114 Photoreactivation, 114 Photorespiration, 686 687 Photosynthesis, 32 33, 81, 83 84, 111 112, 187 188, 498, 563, 628, 630 631, 695 Photosynthetic activity, stomatal conductance and, 53 Photosynthetic apparatus, nanoparticle application and, 630 632 Photosynthetic efficiency, 28 Photosynthetic performance under water deficit, 186 187 Photosystem I (PSI), 241, 245 Photosystem II (PS II), 110 111, 241, 245 Phragmites communis, 29t PHT1 genes, 127 128 PHT2 genes, 131 132 Physcomitrella patens, 515 516 Physiological drought, 51 52 Phytaspase, 7 Phytic acid, 376 377 Phytin, 376 377 Phytoaccumulation. See Phytoextraction Phytochelatins (PCs), 226, 276, 433 Phytochelatin synthase (PCS), 226 Phytodegradation, 221 Phytoene desaturase (PDS), 246 Phytoextraction, 222 Phytohormonal content, modifications in, 365 366

985

Phytohormonal signaling under abiotic stress, 397 466 abscisic acid, 399 400 biosynthesis, 400 402 signaling, 402 abscisic acid dependent signal transduction, 402 405 abscisic acid independent signal transduction, 405 auxin (AUX), 406 biosynthesis, 406 407 signaling, 407 408 brassinosteroids (BRs), 409 biosynthesis, 409 410 signaling, 410 413 cytokinin (CK), 420 biosynthesis, 420 421 signaling, 421 423 ethylene (ET), 413 biosynthesis, 413 signaling, 413 416 gibberellins (GAs), 416 biosynthesis, 417 418 signaling, 418 419 jasmonic acid (JA), 423 424 biosynthesis, 424 425 signaling, 426 428 karrikins (KARs), 436 signaling, 437 nitric oxide (NO), 429 430 biosynthesis, 430 431 signaling, 431 433 phytohormone signaling, cross talk between, 437 443 salicylic acid (SA), 423 424 biosynthesis, 426 signaling, 428 429 strigolactones (SLs), 433 biosynthesis, 434 signaling, 434 436 Phytohormone production, 92, 866 867 Phytohormones, 397 399, 543 576, 817 818 biosynthesis and signaling pathways, 544 556 abscisic acid (ABA), 548 auxin, 547 548 brassinosteroids (BRs), 549 550 cytokinins (CKs), 550 551 ethylene, 552 553 gibberellic acid (GA), 551 552 jasmonic acid, 553 554 salicylic acid, 554 556 cross talk between phytohormone signaling, 437 443 future perspective, 564 568 generation of, 371

986 Phytohormones (Continued) -mediated modulation in plant under certain abiotic stresses, 558 564 heavy metal stress, 559 561 salt stress, 563 ultraviolet-B stress, 563 564 water stress, 561 563 production of, 359 361 production of, 558f regulatory mechanism of, 556 558 Phytoremediation, 219 222 phytodegradation, 221 phytoextraction, 222 phytostabilization, 222 phytostimulation, 221 phytovolatilization, 222 rhizofiltration, 222 Phyto-serotonin, biosynthesis of, 776 778 Phytostabilization, 222 Phytostimulation, 221 Phytovolatilization, 222 Picea abies, 667 Picolinafen, 246 PIF (phytochrome-interacting factor), 412 PIF7, 814 815 PIN2 (proteinase inhibitor 2) transcripts, 426 428 Pinitol, 759 Pinus, 515 516 Pinuspersica, 470 Pinus yunnanensis, 565t PIP1 gene, 648 650 PIP2 gene, 649 650 PIP genes, 649, 652 PIPs (plasma membrane intrinsic proteins), 517 Piriformospora indica, 128, 131 Pisum sativum, 11t, 29t, 37 38, 565t, 868 869 Pityrogramma calomelanos, 222 PIWI (P element induced wimpy testis)-interacting RNAs (piRNAs), 719 720 PIWI domain, 471 Planococcus rifietoensis, 363 364 Plant-breeding programs (PBPs), 890 Plant cells, 1 Plant growth-promoting (PGP) capabilities, 862 Plant growth-promoting rhizobacteria (PGPR), 48, 59 60, 84 85 Plant ion response to stresses, 826 Plant microbe interactions in plants and stress tolerance, 355 drought stress, 364 367 future prospects, 380 383 heavy metal toxicity stress, 367 373 mineral nutritional imbalance stress, 373 380

Index

salinity stress, 358 364 Plant nutrients uptake, increase in, 361 Plant single-cell systematic biology, 611 612 Plant stress physiology, 779 Plasma-membrane intrinsic proteins (PIPs), 644 646 Plastoquinol (PQH2), 297 Plastoquinone, 246 247 Plectranthus scutellarioides, 29t Poaceae, 222 POLARIS, 818 Polyamines (PAs), 481 482, 760 761 and abiotic stress tolerance, 481 496 accumulating transgenic plants, 486 488 future perspectives, 491 492 metabolism of, 483 484 in response to different abiotic stresses, 489 490 metal stress, 489 osmotic, salinity, heat, and/or cold stress, 489 490 synthesis of, 482 483 treatment modulated plant-stress tolerance, 490 491 Polyamines biosynthetic pathway, 483f Poncirus trifoliata, 487t Populus balsamifera, 649 Populus simonii X P. balsamifera, 649 Populus tomentosa, 763 Populus trichocarpa, 132 133, 724 Porphyrins, 246 Posttranscriptional gene silencing (PTGS), 469 471 Posttranslational modifications (PTMs), 429, 431, 794 795 Potassium, 38 39, 86 87, 187 188, 377 379, 489 and sugar production, 892 893 Potassium deficiency quantitative trait loci, 928 929 PP2A (protein phosphatase 2A), 411 412 PR1 gene, 426 428 Primary event, 28 32 Primary miRNA (pri-miRNA), 720 Primary root growth, mechanism of changes in, 125 Principal component analysis (PCA), 588 589 Progesterone, 549 550 Programmed cell death (PCD), 1, 2t, 167 168 flooding-induced, 10 11 heavy metal- and nanoparticle-induced, 13 16 plant proteases involved in, 6t reactive oxygen species and, 3 6 -related proteases, 6 8 salinity-induced, 12 ultraviolet-induced, 12 13 Programmed cell death related proteases, 6 8 Proline, 55 56, 243 244, 758 Promicromonospora sp., 359 361, 363 Protein complexes of photosystem I, 256 257 Protein oxidation, 242

Index

Protein phosphorylation, 518 519 Protein protein interaction networks, 590 591 Protein S-nitrosylation, 796 under adverse environmental stress conditions, 795 799 extreme temperatures, 796 797 heavy metals, 798 799 ozone, 799 salinity, 798 wounding, 797 Protein stability, regulation of, 525 529 calmodulin-mediated alterations, 529 hormone-mediated stress tolerance in plants, 526 528 abscisic acid, 527 528 auxin, 526 brassinosteroids, 526 527 gibberellins, 527 ubiquitin protease system, 528 Protein synthesis, 87, 563 Protein tyrosine nitration (NO2-Tyr), 794 795 Protein tyrosine nitration during abiotic stress situations, 799 801 extreme temperatures, 800 heavy metals, 801 salinity, 801 wounding, 801 Proteomic analyses, 799 800 Proteomic modifications of plants exposed to nanoparticles, 307 308 Proteomics, 513 542, 584 585 future aspects, 531 novel proteins, synthesis of, 530 organelle proteins, overexpression of, 529 530 protein stability, regulation of, 525 529 calmodulin-mediated alterations, 529 hormone-mediated stress tolerance in plants, 526 528 ubiquitin protease system, 528 proteins and genes associated with signaling cascades and transcriptional regulation, 515 516 proteins and genes with roles in protection of membranes, 516 proteins involved in water and ion uptake and transport, 517 reactive oxygen species (ROS) on protein modification, 517 525 carbonylation, 524 525 glutathionylation, 523 524 histone, 520 521 nitrosylation, 525 posttranslational modifications, 518 520

987

sulfonylation, 522 523 tryptophan oxidation, 524 tubulin, 521 522 Proteus sp., 863t Protoporphyrinogen oxidase (PROTOX), 246 PRR5 gene, 813 PRR7 gene, 813 Prr7 mutant, 813 PRR7 regulation, 817 PRR9 gene, 813 PsbA, 112 113 Pseudomonas, 356, 359, 362, 365 366, 378, 866 867, 870, 872t Pseudomonas aeruginosa, 863t, 872t Pseudomonas aurantiaca, 359 361 Pseudomonas chlororaphis, 365 366, 869 Pseudomonas extremorientalis, 359 361 Pseudomonas fluorescens, 359, 361, 871 872, 872t Pseudomonas mendocina, 363 364 Pseudomonas moraviensis, 871 Pseudomonas pseudoalcaligenes, 363 Pseudomonas putida, 90 91, 225 226, 359 361, 367, 863t, 869, 871 872 Pseudomonas sp., 90 91, 366 367, 863t, 872t Pseudomonas strains, 872t Pseudomonas stutzeri, 872t Pseudomonas syringae, 363 364, 428, 866 867 Pseudomonas syringae pv. tomato, 785 786 Pseudomonas tolaasii ACC23, 872t Pteris cretica, 222 Pteris longifolia, 222 Pteris umbrosa, 222 Pteris vittata, 697 698, 842 843 P-type 5 ATPase, 125 Pulse crops, yield responses under drought, 923 Putative zinc finger proteins, 827 P-utilization efficiency (PUE), 124 Putrescine (Put), 481 482 Pyrimidine, 112 113 Pyrimidinone dimers, 112 113 Pyrimidinylthio (or oxy)-benzoates, 245 246 Pyrococcus furiosus, 530 Pyrus calleryana, 226 Pyrus communis, 486 488, 487t Pyruvate, 400 Pyruvate dehydrogenase 2, 254 255 Pyruvate orthophosphate dikinase, 689 690 Pyruvate P1 dikinase, 28 32

Q QRT-PCR technique, 830 QTL mapping, 838 839

988 Quantitative trait loci (QTL), 159 160, 164 165, 581 583, 826, 917 confidence interval (CI), 917 918 for developing stress tolerance in plants. See Abiotic stress, types of identification, 944 945 mapping, 838 839, 917, 944 945 metaanalysis, 917 918 QTL cluster, 917 918 Quercus suber L., 189 190

R RAB18, 813 Radial oxygen loss (ROL), 162 Radiation effect of, 109 113 biochemical changes, 111 112 molecular damages, 112 113 morphological and physiological effects, 110 111 types and sources of, 107 109 alpha radiation, 108 beta radiation, 108 gamma radiation, 108 109 ultraviolet radiation (UVR), 109, 115t X-rays, 109 Radiation stress, 105 107 mitigating strategies, 113 119 endogenous strategies, 114 plant hormones as protectants against harmful radiation, 118 119 transduction of signal via ultraviolet damage, 117 118 ultraviolet-B, 117 ultraviolet shielding and behavioral escape mechanisms, 114 116 source of life on earth, 107 Raf, 415 Raffinose, 505 506, 939 of oligosaccharides, 757 758 Rainfall, deficiency of, 79 Ralstonia metallidurans, 227 Raphanus sativa, 526 527 Raphanus sativus, 15t, 560 561, 565t Ra-siRNAs, 469 Ratio of deep rooting (RDR), 922 923 RbcL, 112 113 RbcS, 112 113 RD22 proteins, 305 RD29A, 415 416, 813 RdreB1Bl gene, 649 Reactive nitrogen species (RNS), 331, 517 518, 793 795, 802

Index

Reactive oxygen species (ROS), 2 5, 25 27, 32 35, 37f, 53 54, 78, 84 85, 108 109, 111 112, 116, 118, 177, 210, 241 244, 358, 475, 485 486, 671, 687, 723, 763, 825 826 and programmed cell death, 3 6 Reactive oxygen species (ROS) on protein modification, 517 525 carbonylation, 524 525 glutathionylation, 523 524 histone, 520 521 nitrosylation, 525 posttranslational modifications, 513 514, 518 520 acetylation, 519 520 glycosylation, 519 phosphorylation, 518 519 succinylation, 520 sulfonylation, 522 523 tryptophan oxidation, 524 tubulin, 521 522 Reactive oxygen species (ROS) regulations, 323 354, 324t antioxidants involved in stress-induced regulation of, 333 339, 334f enzymatic antioxidants, 334 337 nonenzymatic antioxidants, 337 339 future prospects, 343 344 in plant organelles during abiotic stress, 326 333 apoplasts, 331 332 chloroplasts, 328 329 mitochondria, 329 330 peroxisomes, 330 331 ROS-regulated MAPK proteins, 827 signaling roles of ROS in plants under abiotic stress, 339 343 ROS signal perception, 339 340 transduction and interaction of ROS signaling, 340 343 Receptor-like kinase (RLK), 399 Receptor-like/pelle kinases (RLKs), 5 6 Recombinant inbred lines (RILs), 838 839, 917, 920 921 Recombinant organism, 223 Red mangrove, 53 Redox regulation, nanoparticle application and its role in, 628 630 Reduction, 682 683 Regeneration, 683 Relative water content (RWC), 686 687 Respiration, 32 33 Rhamnaceae, 51 52 Rhizobacteria, 59 60, 358, 861 882 direct mechanism, 865 867 ACC deaminase production, 867

Index

N2 fixation, 865 phosphate solubilization, 865 866 phytohormone production, 866 867 siderophore production, 866 growth attributes by plant growth-promoting rhizobacteria, 862 indirect mechanism, 867 874 impact of nanoparticles stress over rhizobacteria, 869 rhizospheric bacteria in abiotic stress, 870 874 root exudation strengthening synergy with rhizobacteria, 868 869 mode of action for PGPR, 862 865 Rhizobium, 356, 362, 367, 866 869, 872t Rhizobium tropici, 362 Rhizofiltration, 222 Rhizophora mangle, 53 Rhizosphere, 355 356 Rhizospheric bacteria in abiotic stress, 870 874 Rhodococcus sp., 872t Rhodopseudomonas palustris, 225 226 Ribose-5-phosphate isomerase, 686 Ribosomal RNA, 467 468 Ribosylation, 513 514 Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), 7 8, 426 428, 683, 692, 695, 701 702, 796 797, 939 Ribulose-5-phosphate 3-epimerase (RPE), 685 686 Ribulose bisphosphate (RuBP), 77 78 Rice (Oryza sativa L.), 515 516, 581 583 Al tolerance in, 932 933 BC inbred lines in, 940 941 cold tolerance, 938 genetic control of heat tolerance in, 937 iron toxicity tolerance in, 934 935 salt tolerance, 940 Ricinus communis, 515 516 Rimsulfuron, 242 RNA-dependent RNA polymerase (RDRs), 468 469, 471 472 RNA interference (RNAi), 467 468 RNA polymerase II (RNA pol II), 469 RNase III, 470 471 Root-adhering soils (RAS), 363 364 Root-colonizing bacteria, 90 91 Root exudation strengthening synergy with rhizobacteria, 868 869 Root growth modification, 92 93 ROOT HAIR DEFECTIVE-LIKE1 (RSL1), 126 ROOT HAIR DEFECTIVE-LIKE2 (RSL2), 126 Root hairs, mechanism of changes in, 126 Root responses under drought, 922 923 Root system architecture (RSA), 123 125

989

Rosmarinus officinalis L., 299 300 RSL2 genes, 126 RUBISCO, 501 RuBisCO activase (RCA), 693 694 RuBisCO protein, 28, 688 Rumex crispus, 162 163 Rumex palustris, 163

S Saccharomyces cerevisiae, 132 133, 226, 842 843 Saccharomy cescerevisiae, 486 488, 487t Saccharum barberi, 251 Saccharum edule, 251 Saccharum officinarum, 29t, 251 252 Saccharum robustum, 251 Saccharum sinense, 251 Saccharum spontaneum, 251, 254 S-adenosyl-L-methionine (S-AdoMet), 413 S-adenosyl methionine (S-AdoMet) synthetase, 165 166, 413, 552 553 S-adenosylmethionine decarboxylase (SAMDC), 482 483, 487t Salicornia brachiata, 529 530 Salicylic acid (SA), 56, 92, 167 168, 281 282, 338 339, 341 343, 398 399, 423 424, 426f, 543 546, 545t, 554 556, 558, 785, 816 818 biosynthesis, 426 signaling, 428 429 Saline sandy loam soil, 63 Saline soils, 48 50 classification of, 49 50 genesis of, 48 49 sources of, 49 Salinity, 563, 579 581, 740 742, 843, 873 874, 888 889 Salinity and its tolerance strategies in plants, 47 biochemical adaptation, 54 57 hormone regulation, 55 57 intercellular signaling, 54 55 osmotic regulations, 54 oxidative modification, 54 cellular mechanisms, 57 58 Na1 exclusion from the cell, 57 Na1 transporters, 57 58 effect of different amendments in tolerance against salinity, 62 63 inorganic amendments, 63 organic amendments, 62 63 genetic engineering of halotolerant plants, 63 64 genetic modification in plants to enhance tolerance against salinity, 63 microbe plant interaction, 59 62 fungal plant interaction, 61 62 halotolerant microbe mediated processes, 60 61

990 Salinity and its tolerance strategies in plants (Continued) plant growth-promoting rhizobacteria, 59 60 osmotic deregulations, 51 52 physiological adaptation, 52 53 stomatal conductance and photosynthetic activity, 53 plants and salt stress, 48 soil physical and chemical properties effect on salinity on, 51 effect on sodicity on, 50 51 specific ion toxicity, 52 tissue tolerance to ions, 58 59 apoplastic alkalization and reacidulation, 59 compartmentation of Na1 inside cell, 58 homeostasis, 59 Salinity-induced programmed cell death, 12 Salinity stimulated PAs, 489 490 Salinity stress, 12, 358 364, 517, 525, 665, 940 942 aquaporins in, 650 651 -induced ethylene production, 361 plant growth promoting rhizobacteria and alleviation of, 359 364 antioxidative enzymes, induction of, 363 decreased salinity stress induced ethylene production, 361 exopolysaccharides (EPS), production of, 363 364 ion homeostasis in plants, 362 363 osmolytes, accumulation of, 362 phytohormones, production of, 359 361 plant nutrients uptake, increase in, 361 systemic tolerance, induction of, 364 Salt-affected soils, 48 49 Salt overly sensitive (SOS) proteins, 812 813, 844 846 Salt overly sensitive 1 (SOS1), 650 Salt overly sensitive 2 (SOS2), 650 Salt overly sensitive 3 (SOS3), 650 Salt stress, 255 257, 489 490, 504 505, 563, 616 617, 633, 691 693, 740 741, 798 circadian clock regulating plant response to, 812 813 ionomics of, 845 846 HKT-type Na1 transporters, 846 V-type H1 ATPases, 846 late-embryogenesis-abundant- type proteins in, 844 845 microRNA and, 724 725 plant response to gene regulation and transcriptional factors in, 826 827 and plants, 48, 843 sRNAs in alleviating, 474 tolerance to, 665

Index

Salt-stressed chickpea plants (Cicer arietinum L. cv. Gokce), 336 337 Salt-stressed eggplant plants (Solanum melongena Mill.), 338 339 Salvia officinalis, 664 665 SAMDC1, 483 484 SAMDC2, 483 484 Saponin, 785 SAR (systemic acquired resistance), 428 SA-reactive oxygen species (SA-ROS), 558 Sarkaran, 258 259 SAS (shade avoidance syndrome), 439 Saspases, 7 8 Sauromatum guttatum, 554 555 SBPase, 693 SCARECROW, 125 Scdr1 (sugarcane dry-responsive 1), 258 SCF (SKP1, CULLIN, F-BOX) E3 ubiquitin-ligase complexes, 551 552 Schizosaccharomyces pombe, 226 Scytonemin, 114 116 Secondary event, 28 32 Secondary metabolites, 663 666, 668f, 670 Sedoheptulose-bisphosphatase (SBPase), 684 Sedum alfredii, 222, 672 Seed germination, 499, 561 562 Selaginella moellendorffii, 515 516 Selenium, 39 toxicity, 934 Semimetals, 207 208 Senescence, 498 499 Sensor proteins, 500 Serotonin, 761 762, 775, 778 779, 781, 784 785 Serotonin N-acetyltransferase (SNAT), 776 777 SERRATE (SE), 720 Serratia, 356, 863t, 872t Sesbania rostrata, 167 Sesuvium portulacastrum, 651 71:13, 836 837 Shikimate phenylpropanoid pathway, 701 Shoot apical meristem, 474 SHOOTMERISTEMLESS1 gene, 721 722 ShSUT1, 264 ShSUT2, 264 ShSUT4, 264 Siderophore production, 866 Siderophores, 275 276 generation of, 368 370 Signal-transduction cascades, 501 502 Sinapis alba, 179 180 Sinapoyl serotonin, 778 779 Single-cell biology approach, need of, 611 612 Single-cell genetic (SCG) analysis, 615

Index

Single-cell genomic analysis, 619 620 Single-cell models, 612 614. See also Abiotic stress, single-cell response to guard cells, 612 613 male and female gametophytes, 612 trichomes, 613 614 Singlet oxygen, 3 Sinorhizobium, 359 Sinorhizobium meliloti, 760 761 SK1 gene, 164 165, 168 169 SK2 gene, 164 165, 168 169 SKIP expression, 814 815 SKP2A (S-PHASE KINASE-ASSOCIATED PROTEIN 2A), 407 408 SLT1 F-box proteins, 551 552 Slurry-phase bioremediation, 217 Small, basic intrinsic proteins (SIPs), 644 646 Small interfering RNAs (siRNAs), 467 469, 471, 719 720 S-methylmethionine (SMM), 485 486 SNAC1 gene, 581 583 S-nitrosoglutathione (GSNO), 736, 742, 795 797 S-nitroso-N-acetylpenicillamine (SNAP), 741 742 S-nitrosothiols (SNOs), 795 798 S-nitrosylation, 517 518, 522, 744, 794 796, 798 799 SNORKEL1 (SK1) gene, 159 160 SNORKEL2 (SK2) gene, 159 160 Sodicity, 50 51 Sodium nitroprosside (SNP), 57, 740 741 Software and algorithms for plant systems biology, 593 595 data handling and analysis, 594 storage and maintenance of data and results, 594 595 visualization of plant omics data, 594 Soil biota activity, 84 85 Soil infiltration rates, 85 Soil physical and chemical properties effect on salinity on, 51 effect on sodicity on, 50 51 Soil physicochemical activities, 85 Soil salinity, 47 48 Soil salinization, 47 48, 888 Solanum lycopersicum, 29t, 58, 61 62, 290, 293, 300 304, 310 311, 330, 471, 473t, 487t Solanum melongena, 29t, 338 339, 487t, 565t Solanum nigrum, 14t, 191 192 Solanum tuberosum, 29t, 294, 694, 756 757 Solar radiation, 12 13, 105 107 Solid-phase bioremediation, 217 Soluble protein, 82 Soluble sugars, 497 499, 503 504 Sorbitol, 759

991

Sorghum, 515 516 Sorghum bicolor, 757 Southeast Mediterranean Sea management of impacts of abiotic stress in, 891 897 Soybean (Glycine max), 124 125, 515 516 Al tolerance in, 933 SPDS1, 483 484, 487t SPDS2, 483 484 Spd synthase (SPDS), 482 Specific ion toxicity, 52 Spermidine (Spd), 481 482 Spermine (Spm), 481 483 Sphingomonas desiccabilis, 225 226 Spinach (Spinacia oleracea L.), 335 336 Spinacia oleracea, 335 336, 485 486 Spindyl (SPY), 419 SQUAMOSA PROMOTER BINDING PROTEIN-LIKE family, 721 722 SR160, 549 550 sRNAs, 468 469 in alleviating salt stress, 474 biogenesis and mechanism of action of, 469 in the development of leaf and leaf size and morphology, 474 -mediated gene regulation, 469 471 posttranscriptional gene silencing, 470 471 transcriptional gene silencing, 470 in oxidative stress regulation, 475 in signaling of hormone, 476 in vernalization, 472 474 SSR markers, 933 934 Stable QTL (sQTL), 917 Stachyose, 505 506, 757 758 Stanford Microarray Database, 583 584 Starch, 757 Staurosporine, 501 Stay-green, 943 Stenotrophomonas maltophilia SBP-9, 863t Stevia rebaudiana Bertoni, 760 761 Stomata, 83 84, 688, 690 691 Stomatal conductance and photosynthetic activity, 53 Storage and maintenance of data and results, 594 595 Streptomyces sp., 863t, 872t Stress, 8 16 defined, 779 signaling of, 85 Stress ethylene, 357, 366 Stress hormone, 399 Stress-induced ethylene production, 366 Stress-induced regulation of ROS, antioxidants involved in, 333 339 enzymatic antioxidants, 334 337 nonenzymatic antioxidants, 337 339

992 Stress proteins, 87 Stress related genes, activations of, 558f Stress-resistant crops, developing, 943 944 Stress-responsive genes, circadian clock regulating, 815 816 Stress-responsive signaling pathways, 530 Stress signaling, 88 Stress tolerance, 305 307 breeding for, 890 Stress tolerance, abiotic, 467 480 mRNAs in, 471 small interfering RNAs in defense against pathogen, 471 472 sRNAs, 468 469, 475f sRNA-mediated gene regulation, 469 471 in alleviating salt stress, 474 in the development of leaf and leaf size and morphology, 474 in oxidative stress regulation, 475 posttranscriptional gene silencing, 470 471 in signaling of hormone, 476 transcriptional gene silencing, 470 in vernalization, 472 474 sRNAs, biogenesis and mechanism of action of, 469 Strigolactones (SLs), 398 399, 433, 434f, 435f, 543 544, 545t biosynthesis, 434 signaling, 434 436 Sub1A gene, 160, 168 Sub1B gene, 168 SUB1 gene, 169 Submergence escape strategy under, 159 160 quiescence strategy under, 160 Submergence 1 (Sub 1), 159 160 Submergence tolerance mechanisms, 159 160, 161f Subtilisin-like serine proteases, 7 Succinylations, 513 514, 520 Succulent strategy, 686 687 Sucrose, 498, 507 Sucrose-6-P synthase (SPS), 264 Sucrose-phosphate synthase, 503 504 Sucrose-P phosphatase (SPP), 264 Sucrose synthesis and partitioning during abiotic stress, 264 266 SUCROSE TRANSPORTER 2 (SUC2), 142 Sugar alcohols (polyols), 759 alditols, 759 cyclitols, 759 Sugar beet, 892 893 Sugar beet PSD, 893t Sugarcane (Saccharum officinarum L.), 251, 254 255 and beet processors, 895t

Index

Sugar crops, 893 Sugars, 142 Sugar sensing and signaling, 500 501 Sugars’ role in regulation of environmental stress, 497 512 future perspectives, 507 plant growth and development, 498 in processes of plants physiology, 498 500 flowering, 499 hypocotyl growth, 500 photosynthesis, 498 seed germination, 499 senescence, 498 499 signal-transduction cascades, 501 502 sugars and abiotic stress interaction in plants, 502 507 light, effects of, 505 low temperatures, effects of, 505 506 oxidative stress and antioxidant system, 506 507 salinity, effects of, 504 505 water deficit, effects of, 502 504 sugar sensing and signaling, 500 501 Sulfonylamino-carbonyltriazolinones, 245 246 Sulfonylation, 513 514, 517 518, 522 523 Sulfonylureas, 245 246 Sulfooquinovosyldiacylglycerol (SQDG), 143 Sulfur compounds, 276 Sulfur metabolism, 471 Sumoylation, 513 514 Superoxide dismutase (SOD), 26 27, 84 85, 475, 485 486, 556 Superoxide dismutase, 243 Sustainable agriculture, 874 Symbiotic bacteria, 865 Synechococcus, 737 738 Systemic acquired acclimation (SAA), 341 343 Systemic acquired resistance (SAR), 870 871 Systemic tolerance, induction of, 364

T Taipei 309, 829 830 Tamarix androssowii Litv., 334 335 TaMnSOD activity, 334 335 TaPHT3, 132 133 TAS14 gene, 304 305 Temperature, 885 887 Temperature stress, 693 695 high temperature, 693 694 low temperature, 694 695 microRNA and, 725 726 resistance mechanism of medicinal and aromatic plants to, 668 669 Temperature stress regulation in plants, 25

Index

heat stress, plant adaptations to, 33 39 biochemical adaptation, 34 35 molecular adaptation, 35 36 nutrient management approach, 36 39 physiological adaptation, 33 34 high temperature, 27 28 low temperature, 28 33 Tetradenia riparia, 762 763 Thale cress (Arabidopsis thaliana), 581 583 Thellungiella halophila, 13t Thellungiella halophilais, 695 Thermospermine (tSpm), 481 482 Thermus thermophilus, 489 490 Thiobarbituric acid (TBARS), 297, 506 507 Thioredoxin (TRX), 429 Thlaspi caerulescens, 222, 672 Thlaspi goesingense, 280 Thlaspi species, 222 Thymus daenesis, 664 Thymus vulgaris, 664 TIP genes, 652 TIPs (tonoplast-intrinsic proteins), 517 Tir1/afb2 Arabidopsis mutant, 408 Tir1afb2 mutants, 441 Tissue tolerance to ions, 58 59 solute accumulation in cells, 58 59 apoplastic alkalization and reacidulation, 59 compartmentation of Na1 inside cell, 58 homeostasis, 59 Titania NPs, 869 Titanium NPs (nTi), 631 632 Titanium oxide, 630 Tobacco (Nicotiana tabacum), 25 26 TOC1 expression, 813 818 Tocochromanol, 297 Tolerance strategy, 26 27, 33 34 Tolerance to Pi deficiency (TPDE), 927 928 Tolerating genes, induction of, 826 827 Tomato (Solanum lycopersicum), 941 942 TONOPLAST INTRINSIC PROTEIN (TIP), 644, 646 Toxic heavy metals, 182 185 cadmium, 182 chromium, 184 185 lead, 182 183 mercury, 183 184 Toxic metals detoxification of, 220t genetic engineering and its application in bioremediation of, 223 227 arsenic, 225 226 cadmium, 226 lead, 227 mercury, 224 225

993

remediation of toxic metals and metalloids, 215 216 TPS1 gene, 266 TPS2 gene, 266 Trace element transport and heavy-metal toxicity, aquaporins in, 652 654 Trans-acting siRNAs (ta-siRNAs), 468 469 Transcriptional gene silencing (TGS), 470 Transcriptional regulatory networks, 591 592 Transcriptional reprogramming, 471 Transcription factors (TFs), 123 124, 135 136, 137t, 398 399, 784, 827 828 binding to promoters, 828 829 Transcriptomic modifications by nanoparticles and abiotic stress, 304 307 Transcriptomics, 583 584 Transfer RNA, 467 468 Transgenics, 648 649 Transition metals, 840 Transketolase, 685 Trans-nitrosylation reaction, 795 TRANSPORT INHIBITOR RESPONSE1 (TIR1), 126 Transportinhibitor response 1 (TIR1), 476 TRANSPORT INHIBITOR RESPONSE1, 721 722 Trans-Zeatin (tZ) biosynthetic pathway, 421, 421f Trehalose, 499, 756 757, 843 844 Trehalose-6-phosphate (T6P) synthase (TPS), 252 253 Triazolopyrimidines, 245 246 Trichoderma asperellum Q1, 872t Trichomes, 613 614 Trifolium repens L., 334 335 Trifolium vulgaris, 868 869 Trigonella sp., 565t Triose-phosphate isomerase (TPI), 685 Triplet oxygen, 3 Triticum aestivum, 10t, 11t, 15t, 29t, 56, 293, 337 339, 359, 473t, 485 486, 487t, 648 649, 651 Triticum spp. L., 307 308 Triticum turgidum, 654 655, 930 salt tolerance QTLs in, 941 Tryptamine 5-hydroxylase (T5H), 776 777 Tryptophan biosynthetic pathway, 524 Tryptophan decarboxylase (TDC), 776 777 Tryptophan metabolism, 776 778 Tryptophan oxidation, 513 514, 524 Tsc10a-1, 836 837 Tubulins, 513 514, 521 522 Typhasterol, 409 410

U Ubiquitin, 528 Ubiquitination, 513 514 Ubiquitin protease system, 528 Ultraviolet-B stress, 563 564

994

Index

Ultraviolet-induced programmed cell death, 12 13 Ultraviolet light, 666 Ultraviolet radiation (UVR), 105 107, 109 111, 114 116, 115t, 119 Uncategorized X intrinsic protein (XIP), 644 646 Ustilago maydis, 485 486 UV-B radiation, microRNA and, 725 UV-B stress, 701 703 UV radiation, 565t

V Vacuolar phosphate transporter 1 (VPT1), 134 Vacuolar processing enzyme (VPE) activity, 2, 7 proVPE, 7 Variovorax boronicumulans strain CGMCC 4969, 866 867 Variovorax paradoxus, 361, 366, 872t Vernalization, 26 27 Vernalization, sRNAs in, 472 474 Vicia faba L., 784 785 Vigna mungo L., 189 190 Vigna radiata, 489 490, 523 524, 560 561, 631, 745 Vigna unguiculata, 9, 279 280 Viminaria juncea, 167 Viola calaminaria, 222 Violaceae, 222 9-cis-Violaxanthin, 401 Visualization of plant omics data, 594 Vitis vinifera, 29t, 762 763 Volcanic eruption, 213 214 V-type H1 ATPases, 846

W Water, 81 82 loss of, 80 Water-deficient lipids, 88 Water deficit growth attributes of plants affected by, 185 186 and oxygen deprivation, 617 photosynthetic performance under, 186 187 Water-deficit stress, 185 188, 827 828 antioxidative defense mechanism under, 187 combination of metal with, 188 192 on plant growth and physiological processes, 189 190 plant water relations under metal stress, 191 192 osmotic adjustment, 187 188 Waterlogging, 690 691, 942 Waterlogging stress, 157 161, 781 Waterlogging tolerance, 160 162

gene regulation of, 829 830 Water pollution, 559 Water stress, 77 78, 561 563, 686 691 Water-use and photosynthetic activity under drought, 921 922 Water-use efficiency (WUE), 686 687 Wheat plants, 162 Whole-cell oxygen evolution (photosynthesis), 467 468, 476 Wild barley (Hordeum spontaneum), 689 690 Wild soybean alkaline salt tolerance (AST) in, 941 WIPK, overexpression of, 426 428 Wound, 258 259, 262 264 WRKY23 gene, 526 WRKY6, 126 WRKY genes, 515 516

X Xanthine dehydrogenase (XDH), 332 Xanthine oxidase (XAO), 330 332 Xanthoxin, 401 XAP5 CIRCADIAN TIMEKEEPER, 818 X-difluoromethylarginine (DFMA), 490 491 X-difluoromethylornithine (DFMO), 490 491 Xenopus laevis, 644 X-rays, 109

Y Yield responses under drought, 923 924 YODA, 412 YUC2 gene, 526 YUC6 gene, 526 YUCCA flavin-containing monooxygenases, 406 Yule Simpson paradox, 611 612

Z Zea mays, 11t, 29t, 124 125, 293, 338 339, 565t Zeaxanthin epoxidase (ZEP), 167, 401 Zeaxanthin oxidase (ZEP), 527 528 ZFHD gene, 304 305 ZFP245, overexpression of, 581 583 Zinc, 209t, 489, 565t Zinc deficiency quantitative trait loci, 931 Zinc toxicity, 936 Zingiber officinale, 667 Ziziphus mauritiana Lam., 51 52 ZmPHO2, 137 138 Zoysia japonica, 689 ZRT, 842 843