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Copyright © 2009. Nova Science Publishers, Incorporated. All rights reserved. Devane, Robert T.. New Plant Physiology Research, Nova Science Publishers, Incorporated, 2009. ProQuest Ebook Central,

Copyright © 2009. Nova Science Publishers, Incorporated. All rights reserved. Devane, Robert T.. New Plant Physiology Research, Nova Science Publishers, Incorporated, 2009. ProQuest Ebook Central,

BOTANICAL RESEARCH AND PRACTICES SERIES

NEW PLANT PHYSIOLOGY RESEARCH

Copyright © 2009. Nova Science Publishers, Incorporated. All rights reserved.

No part of this digital document may be reproduced, stored in a retrieval system or transmitted in any form or by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in rendering legal, medical or any other professional services.

Devane, Robert T.. New Plant Physiology Research, Nova Science Publishers, Incorporated, 2009. ProQuest Ebook Central,

BOTANICAL RESEARCH AND PRACTICES SERIES

Copyright © 2009. Nova Science Publishers, Incorporated. All rights reserved.

New Plant Physiology Research Robert T. Devane (Editor) 2009. ISBN: 978-1-60741-102-4

Devane, Robert T.. New Plant Physiology Research, Nova Science Publishers, Incorporated, 2009. ProQuest Ebook Central,

BOTANICAL RESEARCH AND PRACTICES SERIES

NEW PLANT PHYSIOLOGY RESEARCH

ROBERT T. DEVANE

Copyright © 2009. Nova Science Publishers, Incorporated. All rights reserved.

EDITOR

Nova Science Publishers, Inc. New York

Devane, Robert T.. New Plant Physiology Research, Nova Science Publishers, Incorporated, 2009. ProQuest Ebook Central,

Copyright © 2009 by Nova Science Publishers, Inc. All rights reserved. No part of this book may be reproduced, stored in a retrieval system or transmitted in any form or by any means: electronic, electrostatic, magnetic, tape, mechanical photocopying, recording or otherwise without the written permission of the Publisher. For permission to use material from this book please contact us: Telephone 631-231-7269; Fax 631-231-8175 Web Site: http://www.novapublishers.com NOTICE TO THE READER The Publisher has taken reasonable care in the preparation of this book, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained in this book. The Publisher shall not be liable for any special, consequential, or exemplary damages resulting, in whole or in part, from the readers’ use of, or reliance upon, this material. Any parts of this book based on government reports are so indicated and copyright is claimed for those parts to the extent applicable to compilations of such works.

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Independent verification should be sought for any data, advice or recommendations contained in this book. In addition, no responsibility is assumed by the publisher for any injury and/or damage to persons or property arising from any methods, products, instructions, ideas or otherwise contained in this publication. This publication is designed to provide accurate and authoritative information with regard to the subject matter covered herein. It is sold with the clear understanding that the Publisher is not engaged in rendering legal or any other professional services. If legal or any other expert assistance is required, the services of a competent person should be sought. FROM A DECLARATION OF PARTICIPANTS JOINTLY ADOPTED BY A COMMITTEE OF THE AMERICAN BAR ASSOCIATION AND A COMMITTEE OF PUBLISHERS. LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA Devane, Robert T. New plant physiology research / Robert T. Devane. p. cm. Includes index. ISBN 978-1-61728-548-6 (E-Book) 1. Plant physiology--Research. I. Title. QK714.D48 571.2--dc22

Published by Nova Science Publishers, Inc. Ô New York

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``2009 2009008031

CONTENTS Preface

vii

Research and Review Chapters Chapter 1

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Chapter 2

Water Deficit Stress-Induced Changes in Higher Plants and Implications for Global Arid Regions Hong-Bo Shao, C. Abdul Jaleel, Fu-Tai Ni, P. Manivannan and R. Panneerselvam Physical and Chemical Signals and their Action in Systemic Responses of Plants to Local Wounding Vladimíra Hlaváčková

1

43

Chapter 3

Root Water Transport Under Abiotic Stress Conditions Ricardo Aroca and Juan Manuel Ruiz-Lozano

Chapter 4

Amino Acids in the Rhizosphere: A Review Rejsek Klement, Formanek Pavel & Vranova Valerie

111

Chapter 5

Harnessing the Bacterial Endophytes for Crop Improvement M. Senthilkumar and M. Madhaiyan

135

Chapter 6

Endoreduplication in Cereal Plants Marina Dermastia

177

Chapter 7

An Overview in Antioxidant Properties of Strawberry Behrouz Ehsani-Moghaddam and Shahrokh Khanizadeh

203

Chapter 8

Marine Photosynthetic Response to Increased Atmospheric CO2 Concentration and Oceanic Acidification Hongyan Wu, Dinghui Zou and Kunshan Gao

217

Fluorescence Response to Temperature Stress in Salt Marsh Taxa of Genus Sarcocornia Under Laboratory Conditions S. Redondo-Gómez, E. Mateos-Naranjo and M. E. Figueroa

229

Chapter 9

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vi

Contents

Short Commentary From Genome to Phenome Primetta Faccioli, Caterina Morcia and Valeria Terzi

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Index

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PREFACE Plant physiology is a subdiscipline of botany concerned with the function, or physiology, of plants. Closely related fields include plant morphology (structure of plants), plant ecology (interactions with the environment), phytochemistry (biochemistry of plants), cell biology, and molecular biology. Fundamental processes such as photosynthesis, respiration, plant nutrition, plant hormone functions, tropisms, nastic movements, photoperiodism, photomorphogenesis, circadian rhythms, environmental stress physiology, seed germination, dormancy and stomata function and transpiration are studied. This book presents the latest research in the field from around the world. Chapter 1 - Water is vital for plant growth, development and productivity. Water deficit stress limits the growth and distribution of natural vegetation and the performance of cultivated plants more than any other environmental factors. Although basic studies and practices aimed at improving water stress resistance and water use efficiency have been carried out for many years, the mechanism involved from molecular level to ecosystem is still not clear. Further understanding and manipulating plant water relations and water stress tolerance at the scale of ecology, physiology and molecular biology can significantly improve plant productivity and environmental quality,which is the basis of agricultural and ecoenvironmental sustainable development.Currently,genomics, post-genomics and metabolimics are very important to explore anti-drought gene resources in different life forms, but modern agricultural sustainable development must be combined with plant physiological measures in field,on the basis of which post-genomics and metabolimics have further a practical prospect.In this review, we have discussed the physiological and molecular insights and effects in basic plant metabolism and drought tolerance strategies under drought condition in higher plants for sustainable agriculture and ecoenvironment in arid and semiarid areas in the world. Chapter 2 - Wounding, caused either by physical injury or by herbivore or insect attack, is one of the most severe plant stresses. Higher plants respond to such stress by initiating various defence-related processes, which include accumulation of defence-related proteins, gene expression, stomata movements and changes in respiration and photosynthesis. These processes take place locally, i.e. in the wounded leaf, but many defence responses were detected also in undamaged leaves distal to the site of wounding (systemic response). This finding indicates that a signal moves from the injured tissue to the distant untreated parts of the plant, where it triggers systemic response. Several kinds of chemical and physical signals have been identified in plants responding to local stress. Despite intensive research, there are

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Robert T. Devane

still many controversial questions about the origin of these long-distance moving signals, their interaction and connection to systemic defence responses. In the following chapter, the main characteristics of physical signals will be discussed together with the mechanism of the generation and propagation of these signals in wounded plants. Methods of electrical signal measurements will be also presented. At the same time, selected chemical signals will be described, with particular focus on the localization of their biosynthesis in plants and their long-distance transport mechanisms after local wounding. An overview of possible interactions between physical (electrical and hydraulic) and chemical (abscisic acid, jasmonic acid, systemin, hydrogen peroxide, ethylene, oligosaccharides, volatiles) signals in long-distance signaling pathways after local wounding will be given and physiological responses of plants to both physical and chemical wound-induced signals will be outlined. Chapter 3 - Plants in nature are constantly exposed to several environmental fluctuations, ranging from changes in light intensities to changes in soil water content. Alterations of almost all environmental factors may potentially cause a water deficit on plant tissues. Such water deficit is caused by the imbalance between leaf transpiration rate and root water uptake. In contrast with the amount of research done dealing with the regulation of leaf transpiration rate during abiotic stresses, studies about root water uptake under abiotic stresses are less abundant and controversy. There are two different water pathways inside the roots. Under normal conditions, the more important pathway is the apoplastic one. This pathway compromises the water flowing through the cell walls and it is governed by the transpiration rate. The second pathway includes the water flowing through the cells, crossing different cellular membranes and it is called “cell-to-cell” pathway. The “cell-to-cell” pathway is governed by the osmotic gradient between the soil solution and the root xylem sap, and it becomes predominant when the transpiration rate is restricted, for example under abiotic stress conditions. Both pathways are regulated to some extent by proteinaceous channels called aquaporins. Plant aquaporins were discovered fifteen years ago, and here we will summarize the most recent knowledge about their involvement in root water uptake under abiotic stress conditions. In general, under these conditions root water uptake diminishes. However, each kind of stress has its specific effects and we will detail herein how different abiotic stresses (drought, cold, salt or flooding) modify root water uptake. At the same time, we will describe how different stress-related plant hormones such as abscisic acid or methyl jasmonate, or molecular signals, i.e. calcium or hydrogen peroxide, also modify root water uptake. From the present data we highlight the importance of the knowledge of how root water uptake is governed under abiotic stress conditions in order to achieve plants more tolerant to such stresses. Chapter 4 - Amino acids are of great significance as regards the study of carbon and nitrogen cycling in soil. These nitrogen compounds, released from roots into the soil, provide N for rhizosphere microflora, react with soil components and, in some cases, can be of significance in direct N-nutrition of plants. In contrast to non-proteinaceous amino acids (phytosiderophores), proteinaceous amino acids have a limited role in nutrient mobilization. In general, amino acids are released from roots via passive diffusion, while their re-uptake is an active process. Exudation sites of particular amino acids can differ within the root system, whereas their re-uptake can occur along the whole length of the root. Amino acid exudation and re-uptake, and the net results of these fluxes, can result in either positive or negative levels of individual amino acids. In this chapter, we discuss factors that influence amino acid

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Preface

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exudation, including age, defoliation, nutrient deficiency, temperature, light intensity, mycorrhizal colonization, diurnal fluctuations, water-deficit stress, concentration around roots, microorganisms, mechanical impedance, elevated [CO2], microbial metabolites, nitrates and aluminum. Alanine, glutamine, aspartic acid, glycine, serine, glutamic acid, proline, lysine, γ-aminobutyric acid, valine, arginine and cystine are the most abundant amino acids in root exudates of C4 plants. In C3 plants, serine, glycine, glutamic acid, alanine, tyrosine, arginine, proline, cystine and aspartate are most abundant. C4 plants exude more glutamine, lysine, γ-aminobutyric acid and valine, while C3 plants exude more tyrosine. Chapter 5 - Microorganism seems to occupy virtually every living and non-living niche on earth. This includes those in the thermal vents, in deep rock sediments, and in desert as well as marine environments. For the purposes of this chapter, this review concentrates on those microorganisms, mostly bacteria that reside in plants. In the past few decades, plant scientists have begun to realize that plants may serve as a reservoir of untold numbers of organisms known as endophytes and efforts are made to isolate endophytes and study their interaction in plants. While there are myriads of epiphytic microorganisms associated with plants, the endophytic ones now seem to be attracting more attention. By definition, these microorganisms (mostly fungi and bacteria) live in the intercellular/intracellular spaces of plant tissues with neutral, beneficial or detrimental interaction. Positive interactions between endophytes and their host plants can result in a range of beneficial effects which includes increased plant growth and development, resistance to disease and to withstand environmental stresses. The ability to successfully manipulate endophytic bacteria in agricultural production systems will depend upon the ability to select, incorporate and maintain beneficial microbial populations in the field. However, much of the basic information regarding endophyte community structure, their principal functions, relative ecological stability, and the organizing forces that govern their continuity, is still lacking. Chapter 6 - Endoreduplication is a variant of the cell cycle whereby cells undergo successive rounds of genome duplication without going through mitosis. It occurs after cells cease the mitotic cycle and the endoreduplicated cells do not re-enter it. As a consequence, endoreduplication leads to an increase of nuclear DNA content and to endopolyploid cells. Although the phenomenon of endoreduplication is widespread among eukaryotes and common in plants, its function is not well understood. Endoreduplication is in many cases, but not exclusively, associated with cell enlargement and increased levels of gene expression. As such it presumably has a role in cell expansion and in increased metabolic activity. In plants, endoreduplication is characteristic of specialized cell types or tissues. In this chapter the molecular mechanisms that regulate endoreduplication will be reviewed and our understanding, albeit very limited, of how endoreduplication is integrated with cereal plant development will be discussed. The specific spatial and temporal distribution of endoreduplication will be shown in different organs of selected cereal plants. Chapter 7 - For the past few years, growing interest has been devoted to the phytochemical content of fruit and specific attention has been given to the antioxidant capacity. Molecules with antioxidant properties play a significant role in several biological processes that sustain life and defense against external stresses. These compounds are known to influence quality, acceptability and stability of foods by acting as flavorants, colorants or antioxidants. The significant variation in antioxidant capacity and total phenolic compounds of selected strawberry cultivars clearly shows that genetics play a major role and also the potential value of breeding to produce certain cultivars with higher amounts of antioxidants.

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During the past several years, new selected strawberry lines were significantly different from the reference variety in terms of total (hydrophilic and lipophilic) and specific antioxidant (superoxide dismutase) capacity. Our studies revealed that these lines are resistant to certain plant diseases, have a good shelf life, and also meet the growing demand from consumers for fruit with higher levels of nutraceutical components. In this chapter, the results of our latest research on antioxidant behavior of some advanced lines and cultivars in strawberry have been discussed. Chapter 8 - Increasing atmospheric CO2 and subsequent rise of pCO2 in seawater alters the carbonate system and related chemical reactions in surface ocean, reducing pH and the concentration of carbonate (CO32-) while increasing that of bicarbonate (HCO3-). Such changes in marine chemistry, with more and more CO2 accumulated in the atmosphere, will be accelerated and affect photosynthetic CO2 fixation processes of phytoplanktonic and macroalgal species in direct and/or indirect ways. Although many unicellular and multicellular species are known to operate CO2-concentrating mechanisms (CCMs) to utilize the large HCO3- pool in seawater, enriched CO2 up to several times the present atmospheric level has been shown to enhance photosynthesis and growth of both phytoplanktonic and macroalgal species that have less capacity of CCMs. Even for the species that operate active CCMs and those whose photosynthesis is not limited by pCO2 in seawater, increased CO2 levels can down-regulate their CCMs and therefore enhance their growth under light-limiting conditions (at higher CO2 level, less light energy is required to drive CCM). Altered physiological performances under high-CO2 conditions may cause genetic alteration in view of adaptation over long time scale. Marine photosynthetic organisms may adapt to a high CO2 oceanic environment so that the evolved communities in future are likely to be genetically different from the contemporary communities. However, most of the previous studies have been carried out without considering the acidifying effects of increased CO2 and other interactive factors. Nevertheless, the advances reported so far are important for us to explore how physiology of marine primary producers performs in a high-CO2 and low-pH oceans. Chapter 9 - We conducted experiments to observe the response of PSII in photosynthetic stems of four Sarcocornia taxa to temperature, under laboratory conditions. Measurements of the parameters of fluorescence were made with fresh stems and then with the same stems after a 24 hours recovery period. All taxa demonstrated sensitivity to both high and low temperatures. Between taxa there were significant differences in the point at which this drop occurred. Sarcocornia fruticosa was the most sensitive to low temperatures and S. perennis ssp. perennis was most sensitive to high ones. The hybrid, S. perennis x fruticosa, showed the greatest tolerance to a range of temperatures. After the 24 hour recovery period, all four taxa demonstrated a loss of fluorescence, indicating permanent damage to PSII, at temperature extremes. The ability of the hybrid to cope with both low and high temperatures under laboratory conditions implies that this taxon has potential to extend its range further north in Europe. The hybrid demonstrated greater tolerance than both parental species, in particular S. fruticosa, to low temperatures. Knowledge about the response to temperature can aid the prediction of how climate change will alter the spacial relationship between taxa. If ambient temperatures increase as predicted, S. perennis ssp. perennis could be displaced by the hybrid. Short Commentary - The introduction of innovative high-throughput analytical techniques and the exponential increase in computer power have moved biology toward new frontiers of research giving the basis for a systems biology-based strategy for crop

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improvement. In such a scenario, plant physiology plays a fundamental role in solving the genotype to phenotype problem, i.e. mapping genes to their function. The basis of such a challenge is a deep integration of the several, different kinds of data/information coming from both “in silico” and dry research and from a wide scientific background. This paper examines the state of such an integration and try to find out what a modern physiologist might need and might provide for getting the best from research activity in the post-genomic era.

Devane, Robert T.. New Plant Physiology Research, Nova Science Publishers, Incorporated, 2009. ProQuest Ebook Central,

Copyright © 2009. Nova Science Publishers, Incorporated. All rights reserved. Devane, Robert T.. New Plant Physiology Research, Nova Science Publishers, Incorporated, 2009. ProQuest Ebook Central,

In: New Plant Physiology Research Editor: Robert T. Devane

ISBN 978-1-60741-102-4 © 2009 Nova Science Publishers, Inc.

Chapter 1

WATER DEFICIT STRESS-INDUCED CHANGES IN HIGHER PLANTS AND IMPLICATIONS FOR GLOBAL ARID REGIONS Hong-Bo Shao

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a

a,b,d*

c

e

c

, C. Abdul Jaleel , Fu-Tai Ni ,P. Manivannan , c and R. Panneerselvam

Shandong Key Laboratory of Eco-environmental Science for Yellow River Delta, Binzhou University, Binzhou 256603,China b Institute for Life Sciences ,Qingdao University of Science & Technology, Qingdao 266042, China c Stress Physiology Laboratory, Department of Botany, Annamalai University, Annamalainagar 608002, Tamil Nadu, India d State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation , Chinese Academy of Science, Yangling 712100, China e College of Life Sciences, Jilin Normal University, Siping 136000, China

ABSTRACT Water is vital for plant growth, development and productivity. Water deficit stress limits the growth and distribution of natural vegetation and the performance of cultivated plants more than any other environmental factors. Although basic studies and practices aimed at improving water stress resistance and water use efficiency have been carried out for many years, the mechanism involved from molecular level to ecosystem is still not clear. Further understanding and manipulating plant water relations and water stress tolerance at the scale of ecology, physiology and molecular biology can significantly *

Author for correspondence Dr. Professor Hong-Bo Shao Institute for Life Sciences, Qingdao University of Science & Technology, Qingdao 266042, China Tel: +86-532-84023984 Email: [email protected] (H.B.Shao)

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Hong-Bo Shao, C. Abdul Jaleel, Fu-Tai Ni et al. improve plant productivity and environmental quality,which is the basis of agricultural and eco-environmental sustainable development.Currently,genomics, post-genomics and metabolimics are very important to explore anti-drought gene resources in different life forms, but modern agricultural sustainable development must be combined with plant physiological measures in field,on the basis of which post-genomics and metabolimics have further a practical prospect.In this review, we have discussed the physiological and molecular insights and effects in basic plant metabolism and drought tolerance strategies under drought condition in higher plants for sustainable agriculture and ecoenvironment in arid and semiarid areas in the world.

Key words: Drought; Water use efficiency (WUE); Antioxidants; Enzymes; Morphology; Gene; Agriculture; Ecoenvironment; Arid region

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1. INTRODUCTION The term stress is used, which is most often subjectively and with various meanings. The physiological definition and appropriate term for stress are referenced as responses in different situations.The flexibility of normal metabolism allows the development of responses to environmental changes, which fluctuate regularly and predictably over daily and seasonal cycles (Figure 1-3). Thus every deviation of a factor form and its optimum does not necessarily result in stress. Stress with a constraint or with highly unpredictable fluctuations imposed on regular metabolic patterns causes injury, disease, or aberrant physiology. Stress is the altered physiological condition caused by factors that tend to alter equilibrium. Strain is any physical and chemical change produced by a stress (Gaspar et al., 2002). Environmental stresses trigger a wide variety of plant responses, ranging from altered gene expression and cellular metabolism to changes in growth rate and plant productivity. Plant reactions exist to circumvent the potentially harmful effects caused by a wide range of both abiotic and biotic stresses, including light, drought, salinity and high temperatures. Among the environmental stresses, drought stress is one of the most adverse factors of plant growth and productivity. The biochemical and molecular responses to drought is essential for a holistic perception of plant resistance mechanism to water limited condition in higher plants (Reddy et al., 2004) (Figure 1, 2). Water stress is the major problem in agriculture and the ability to withstand such stress is of immense economic importance. Water stress tolerance involves subtle changes in cellular biochemistry. It appears to be the result of accumulation of compatible solutes and of specific proteins that can be rapidly induced by osmotic stress (Rhodes,1987). The numerous physiological responses of plant to water deficits generally vary with the severity as well as the duration of water stress (Mathews et al., 1984; Weber & Gates, 1990; Rose et al., 1993; Thakur et al., 1998; Li, 2000; Correia et al., 2001; Pane & Goldstein, 2001; Pita & Pardes, 2001; Weigh, 2001; Shao et al., 2005a-d,2006a-c,2007a-d,2008a-c). Water deficit stress can be defined as situation in which plant water potential and turgor are reduced enough to interface with normal functions (Hsiao, 1973). Water stress is considered to be a moderate loss of water, which leads to stomatal closure, and limitation of gas exchange. Desiccation is a much more extensive loss of water which can potentially lead to gross disruption of metabolism and cell structure and eventually to the cessation of enzyme catalyzing reactions (Smirnoff, 1993). Water stress is characterized by reduction of water

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content, turgor, total water potential, wilting, closure of stomata, and decrease in cell enlargement and growth. Severe water stress may result in arrest of photosynthesis, disturbance of metabolism, and finally dying (McKersie & Leshem, 1994).

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See Reddy et al., 2004 and Shao et al. 2007. Figure 1. Physiological and molecular basis of drought stress tolerance.

Water stress influences plant growth at various levels of cell to community (Smith & Griffiths, 1993). The quantity and quality of plant growth depend on cell division,enlargement and differentiation, and all of these events are affected by water stress (McKersie & Leshem, 1994). Hsiao (1973) concluded that water stress inhibits cell enlargement more than cell division. It reduces plant growth inhibition of various physiological and biochemical processes, such as photosynthesis, respiration translocation, ion uptake, carbohydrates, nutrient metabolism and hormones (Kramer, 1983). Drought stress has adverse influence on water relations in Arachis hypogeae (Babu & Rao, 1983), photosynthesis in peanuts (Bhagsari et al., 1976) and mineral nutrition, metabolism, growth and yield of groundnut (Suther & Patel, 1992). In addition, drought conditions influence the growth of weeds, agronomic management and nature and intensity of insects, pests and diseases in Arachis hypogeae (Wheatley et al., 1989; Wightman & Wightman, 1994). WUE (water use efficiency) is traditionally defined as the ratio of dry matter accumulation to water consumption over a season. Increasing WUE could theoretically affect plant growth. When water is limited, plants that use a finite water supply more efficiently

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would positively affect plant productivity in peanut (Wright et al., 1993). WUE measurements may be made at three levels (i) in single leaf using gas exchange techniques (ii) in whole plants grown in containers and (iii) at the canopy level based on evapotranspiration in the field (Fischer & Turner, 1978).

Figure adopted from http://dragon.zoo.utoronto.ca/~B03T0301D/ABA%20dep.htm http://www.maizegenetics.net/index.php?page=genomics/drought.html Figure 2. Roles of ABA in drought response. Abscisic Acid (ABA) is a regulatory molecule involved in drought stress tolerance. The main function of ABA is to regulate plant water balance through guard cells, and regulate osmotic stress tolerance via cellular dehydration tolerance genes. In addition to drought stress, ABA is also induced by salt, and to a lesser degree, cold stress. ABA-inducible genes have the ABA-responsive element (ABRE) (C/T) ACGTGGC in their promoters.

Variation in WUE amongest or within species can be assessed gravimetrically. However, reliable estimates of WUE, under field conditions may be difficult, owing to the lack of technologies to asses the below ground biomass. But gravimetric technique can be adequately adopted to estimate in genotypic variation in pot culture experiments. Recent studies have shown that carbon isotope discrimination occurring during carbon assimilation by leaves is closely related to WUE in various crops (Farquhar & Richards, 1984; Hubick et al., 1986; Farquhar et al., 1989;Shao et al.2005-2007), suggesting that carbon isotope discrimination technology can be used to screen genotypes for WUE.

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Plant growth and productivity is adversely affected by nature wrath in the form of various abiotic and biotic stress factors. Plants are frequently exposed to many stress conditions such as low temperature, salt, drought, flooding, heat, oxidative stress and heavy metal toxicity (Figure 1-3). Various anthropogenic activities have accentuated the existing stress factor (Mahajan & Tuteja, 2005). Water stress may arise as a result of two conditions, either due to excess of water or water deficit. The more common water stress encountered is the water deficit stress known as the drought stress. The water deficit stress has profound impact on ecological and agricultural systems (Rochefort & Woodward, 1992). The reactions of the plants to water stress differ significantly at various organizational levels depending upon intensity and duration of stress as well as plant species and its stage of development (Chaves et al., 2003). Understanding plant responses to drought is of great importance and also a fundamental part for making the crops stress tolerant (Reddy et al., 2004).

Figure 3. Schematic representation of primary and secondary transport in higher plant cells. Electrogenic H+transport (H+-ATPase in the plasma membrane and vacuolar membrane, H+-PPiase in the vacuolarmembrane) generates gradients of pH and electrical potential difference across the cell and vacuolarmembranes. Na+ ions enter the cell and can be translocated out of the cell or into the vacuole by the action ofa plasma membrane Na+/H+ antiporter (SOS1) or a vacuolar Na+/H+ antiporter (NHX1), respectively (After Blumwald et al., 2004)

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In sunflower, a number of responses to water deficits have been identified which were associated with better performance under drought conditions (Fereres, 1987). One trait, which is potentially very important because of the interactions between temperature and water supply on plant growth, is that of enhanced early vigour (Agurea et al., 1997). Sunflower basal temperatures are higher than that of winter cereal (Villalobos & Ritchie, 1992). There are reports on osmotic adjustment under drought stress in sunflower. Osmotic adjustment can contribute to yield maintenance under pre-anthesis drought conditions in sunflower (Chimneti et al., 2002).

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2. EFFECTS OF WATER DEFICIT ON MORPHOLOGICAL PARAMETERS OF HIGHER PLANTS Growth is one of the most drought sensitive physiological processes due to the reduction of turgor pressure. Cell expansion can only occur when turgor pressure is greater than the cell wall yield threshold. Water stress greatly suppresses cell expansion and cell growth due to the low turgor pressure (McKersie & Leshem, 1994). Mostly plants acclimated to drought by osmotic adjustment. The loss of metabolic activity occurred only at severe stress conditions. The increased stomatal resistance under stress levels indicates the efficiency of the species to conserve water in Albizzia (Meenakshi Sundaravalli et al., 2005). Water deficit reduced the plant growth in pearl millet under drought stress by Kusaka et al., (2005) and in Okra (Bhatt & Srinivasa Rao, 2005). Water is being used economically for growth processes. WUE maintains the better metabolic status of the plant, thus better growth potential in multipurpose agroforestry tree species (Thakur & Kaur, 2001). Various internal and external factors influence growth besides its genetical make up. Growth is an important tool for assessing crop productivity in various crops (Watson, 1952; Radford, 1967; Sestak et al., 1971). Drought at any phenophase can affect almost every aspect of growth of above and below ground parts in multipurpose agroforestry tree species (Thakur & Sood, 2005). Osmotic regulation can enable the maintenance of cell turgor for survival or assist plant growth under severe drought conditions in pearl millet (Kusaka et al., 2005). Crops are exposed to a variety of environmental stresses, viz., drought, salinity or low temperature constitute some of the most serious limitations to crop growth in Helianthus annuus (Chimenti et al., 2002). The reduction in plant height is associated with the decline in the cell enlargement and more leaf senescence in the plant Abelmoschus esculentus under water stress (Bhatt & Srinivasa Rao, 2005).

2.1. Plant Root Length Root characteristics, especially root length, root length density, and the number of thick roots, are important for a plant to have comparatively well established above-ground parts by exploiting the available water in rice (Ekanayake et al., 1985). Drought avoidance due to profound root system that enhances the ability of a plant to capture water is a fundamental adaptation mechanism to drought (Ludlow and Muchow, 1990; Passioura, 1982).

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A prolific root system can confer the advantage to support accelerated plant growth during the early crop growth stage and extract water from shallow soil layers that is other wise easily lost by evaporation (Johansen et al., 1994; 1997). More severe drought stress suggests that the dynamics of root growth under drought conditions might be a key factor to understanding the contribution of roots to drought avoidance (Kashiwagi et al., 2005). Drought stress decreased the root length in Albizzia seedlings (Meenakshi Sundaravalli et al., 2005). Similar results were observed in Erythrina seedlings (Muthuchelian et al., 1986), Eucalyptus microtheca seedlings (Li et al., 2000) and Populus species (Yin et al., 2005). Water stress reduces the biomass of fibrous roots in Avocado cultivars (Chartzoulakis et al., 2002) and in Pearl millet (Kusaka et al., 2005). The root to shoot ratio increases under water stress conditions to facilitate water absorption (Lambers, 1998). The growth rate of wheat and maize roots was found decreased under moderate and high water deficit stress (Nayyar & Gupta, 2006). But the development of root system increases the water uptake and maintains right osmotic pressure through higher proline levels (Djibril et al., 2005). An increased growth was reported by (Tahir et al., 2003) in mango under water stress. The root dry weight was decreased under mild and severe water stress in sugar beet (Mohammadian et al., 2005). A significant decrease in root length was reported in water stressed populus species by Yin et al. (2005). The importance of root systems in aquring water has long been recognized. A prolific root system can confer the advantage to support accelerated plant growth during the early crop growth stage and extract water from shallow soil layers that is otherwise easily lost by evaporation (Johansen et al., 1994, 1997). Past studies report that root to shoot ratio increases under water stress conditions to facilitate water absorption (Lambers et al., 1998) and is related to ABA content of roots and shoots (Sharp & Lenoble, 2002). The root growth was not significantly reduced under water deficits in maize and wheat (Nayyar & Gupta, 2006).

2.2. Plant Stem Length Stem length was decreased in Albizzia seedlings under drought stress (Meenakshi Sundaravalli et al., 2005). Similar results were observed in Erythrina (Muthuchelian et al., 1986), Eucalyptus microtheca seedlings (Li et al., 2000) and Populus species (Yin et al., 2005). Continuous water deficit results in fewer and smaller leaves, which have smaller and more compact cells and greater specific leaf weight in peanut (Chung et al., 1997). Water stress was a very important limiting factor at the initial phase of plant growth and establishment. There was a significant reduction in shoot height in Populus cathayana under deficit stress (Yin et al., 2005). In soybean, the stem length decreased under water deficit stress, but this decreased was not significant when compared to well water control plants (Zhang et al., 2006). The plant height reduced up to 25% in water stressed citrus seedlings (Wu et al., 2006). Stem length was significantly affected under water stress in potato (Heuer & Nadler, 1995).

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2.3. Plant Leaf Area During water stress, total leaf area per plant decreased significantly in Eragrostis curvula (Colom & Vazzana, 2001), Oryza sativa (Cabuslay et al., 2002), Abelmoschus esculentum (Bhatt & Srinivasa Rao, 2005) and in Asteriscus maritimus (Rodriguez et al., 2005). Leaf area plasticity is important to maintain control of water use in crops. In Sorghum, leaf area reduced significantly under water stress. This reduction occurred before stomatal conductance decreased in the remaining viable leaf area (Blum & Arkin, 1984; Blum, 1996). Leaf area was affected adversely in both main shoot and tillers of all the varieties. Reduction in leaf area by water stress is an important cause of reduced crop yield through reduction in photosynthesis (Kramer, 1983). The reduction in plant height and the leaf area under water stress may be associated with the decline in the cell enlargement and more leaf senescence in Abelmoschus esculentum (Bhatt & Srinivasa Rao, 2005). Leaf water potential, osmotic potential and relative water content decreased in stressed plants at all the growth stages in sorghum. The decrease in osmotic potential in response to water deficit was more compared to the leaf water potential at all the growth stages indicating the ability of the leaves to maintain turgor through osmotic adjustment in sorghum (Yadav et al., 2005; Shao et al. 2006). Water deficits reduce the number of leaves per plant and individual leaf size, leaf longevity and leaf reduced by decreasing soil water potential. Leaf area expansion depends on leaf turgor, temperature and assimilating supply for growth, which are all affected by drought in Arachis hypogeae (Reddy et al., 2003). Water deficit stress mostly reduced leaf growth and in turn the leaf area in many species of plants like Populus, Ziziphus etc. (Amdt et al., 2001; Zhang et al., 2004; Yin et al., 2005). Significant interspecific differences between two sympatric Populus species were found in total number of leaves, total leaf area and total leaf biomass under drought stress (Yin et al., 2005). The leaf growth was more sensitive to water stress in wheat, but it was not so in the case of maize (Nayyar & Gupta, 2006).

2.4. Plant Fresh and Dry Weight Prolonged water stress reduced the biomass of fibrous roots in Avocado cultivars (Chartzoulakis et al., 2002). The performance and biomass production potential of trees depend on the maintenance of higher physiological status and economical utilization of resources in agroforestry tree species (Thakur & Sehgal, 2001). Decreased in total dry matter may be due to the considerable decrease in plant growth, photosynthesis and canopy structure as indicated by leaf senescence during water stress in Abelmoschus esculentum (Bhatt & Srinivasa Rao, 2005). Changing resource pools (eg. water or nutrient availability) also may affect the distribution of biomass (Weiner, 1985; Schmitt et al., 1986; Bonan, 1988; Morse & Bazzaz, 1994; Duan & Zhao, 1996; Xin et al., 1998; Wu & Wang, 1999; Pan et al., 2002). Drought stress decreases mean plant biomass and it increases both the relative variation in plant biomass and the concentration of mass within a small fraction of the population. This is supported by earlier studies (Duan & Zhao, 1996; Xin et al., 1998; Wu & Wang, 1999) conducted at single field sites or in pots.

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Drought stress decreased the plant biomass in Cyamopsis tetragonoloba (Shubhra et al., 2003) and spring wheat (Pan et al., 2003). Similar results were observed in earlier studies in wheat (Duan & Zhao, 1996; Xin et al., 1998; Wu and Wang, 1999), Asteriscus maritimus (Rodriguez et al., 2005), and Albizzia seedling (Meenakshi Sundaravalli et al., 2005). Leaf biomass was less in water stressed plants while compared to unstressed plants in the case of tree species (Thakur & Sood, 2005). The reduction in total biomass was reported in groundnut cultivars under water stress due to the reduction in the pod mass rather in the vegetative mass (Nautiyal et al., 2002). Morphological parameters like fresh and dry weights have a profound effect on water limited conditions. There was one by third reduction in fresh and dry weights of Ziziphus rotundifolia plant under drought conditions (Amdt et al., 2001). Progressive drought resulted in a significant reduction in early allocation of dry matter and decreased fresh and dry weight in all plant parts in Populus davidiana (Zhang et al., 2004). Under water deficit stress the biomass production was decreased in Populus cathayana and drought severly affected all growth parameters (Yin et al., 2005). Plant productivity under drought stress is strongly related with the processes of dry matter partitioning and temporal biomass distribution (Kage et al., 2004). A moderate stress tolerance, as shown by dry weight production in transgenic plants, was noticed based on relative shoot growth studies under stress conditions, like drought (Jun et al., 2000). Defoliation resulted from water stress in maize plants resulted in reduced biomass and thin biomass (Yang & Midmore, 2004). Regulated deficit irrigation and partial root drying caused a significant reduction in shoot biomass when compared to control in common bean plants (Wakrim et al., 2005). There was a significant reduction in root dry weight up on induction of drought stress in cotton by PEG (Nepomuceno et al., 1998), there was a significant reduction in shoot dry weight due to water stress treatments in sugar beet genotypes (Mohammadian et al., 2005) and mild stress affected the dry weights of shoots, while shoot dry weight was greater than root dry weight loss under severe stress. Reduced biomass was met with water stressed soybean plants (Zhang et al., 2006). The dry weight of Poncirus trifoliate seedlings decreased to a considerable extent under water stress (Wu et al., 2006).A common adverse effect of water stress on crop plants is the reduction in fresh and dry biomass production (Ashraf and O’Leary, 1996). Reduced biomass production due to water stress has been observed in almost all genotypes of sunflower (Tahir & Mehdi, 2001). However, some genotypes showed better stress tolerance than others. Tahir et al. (2002) evaluated 25 inbred lines of sunflower for drought tolerance. They reported decrease in plant height, leaf area, head diameter, 100-achene weight, yield per plant and plant biomass due to water stress. They further suggested that these traits could be used as a selection criterion for higher yield per plant under water deficit. In a field experiment, Prabhudeva et al. (1998) subjected sunflower genotypes to water stress at bud initiation and/or seed filling stage. They observed that seed and biological yield were reduced most by the imposition of water stress at bud initiation and seed filling stage, than at seed filling stage only.

2.5. Plant Yield Parameters Sunflower yields were higher for winter season than for spring plantings (Gimeno et al., 1989). In early plantings of sunflower, the yield increase was associated with both an increase

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in grain number and in individual grain weight (Soriano et al., 2004). There have been reports on increased yield under water-limited conditions in various plants (Sinclair & Muchow, 2001; Villalobos et al., 1996). Sinclair & Muchow (2001) analysed many physiological and morphological traits that could contribute to an increase in grain yield in drought situations. The portioning of dry matter to the head is critical in the process of yield determination in water stressed sunflower (Sadras et al., 1993). The effect of water deficits on the harvest index of sunflower is complex due to the interactions between the timing and intensity of the stress relative to the developmental processes that determine the components of yield (Soriano et al., 2002). Experiments with sunflower where water deficits were imposed at different growth stages, generated a two- fold difference in harvest index (Soriano et al., 2002). Challenging the view that harvest index may be considered constant over a range of water deficits. Drought during the reproductive stage reduces harvest index (Sadras et al., 1993; Soriano et al., 2002, 2004). The yield components like grain yield, grain number, grain size and floret number were found decreased under pre- anthesis drought stress treatment in sunflower (Chimneti et al., 2002). Water stress greatly reduced the grain yield of maize plants (Yang & Midmore, 2004) and this reduction in grain yield was dependent up on the level of defoliation water stress during early reproductive growth reduces yield in soybean usually as a result of fewer pods and seeds per unit area (Egli & Bruening, 2004). Under non-compact soil conditions, salinity, water logging and saline- watered logged treatments significantly reduced grain yield in wheat genotypes (Saqib et al., 2004). In water stressed soybean the seed yield was far below when compared to well water control plants (Zhang et al., 2006). Seed yield and yield components are severely affected by water deficit. Water stress reduced the head diameter, 100-achene weight and yield per plant in sunflower (Tahir & Mehdi, 2001). These scientists also observed significant but negative correlation of head diameter with fresh root and shoot weight under water stress. Positive and significant relation was recorded between dry shoot weight and achene yield per plant. Reddy et al. (1998) were of the view that water stress for longer than 12 days at grain filling and flowering stage of sunflower (grown in sandy loam soil) was most damaging and reduced the achene yield. Mozaffari & Zeinali (1997) suggested that higher stalk diameter, greater plant height and seed yield are suitable as selection criteria for drought tolerant cultivars. Nandhagobal et al. (1996) subjected sunflower to water stress by skipping irrigation at germination, vegetative stage, button initiation, flowering, and at seed filling stages. Skipping irrigation at flowering stage caused much reduction in yield during summer season. Water stress at flowering also gave the lowest seed oil content.

2.6. Plant Oil Content The seed oil content of sunflower was also affected by changes in environmental conditions. Oil percentage was significantly reduced on the commencement of water stress (Nel et al., 2001), and this reduction in oil yield is increased with increase in water deficit (Kazi et al., 2002). In response to water stress at varying growth stages, oil yield reduction ranged from 41-81% (Kakar & Soomro, 2001). In general, water stress altered the fatty acids

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composition in sunflower. However, composition of saturated fatty acids was less affected due to water stress compared with other fatty acids (Petcu et al., 2000).

3. EFFECTS OF WATER DEFICIT ON BIOCHEMICAL PARAMETERS OF HIGHER PLANTS 3.1. Plant Chlorophyll Content The chlorophyll amount per unit area was higher in water stressed than in well-watered plants in nectarine (Prunus pwesica L. Batsch) plants (Osorio et al., 2006). However the concentration of chlorophyll in the dry matter was lower in water stressed than in wellwatered plants. The chlorophyll content in the wheat leaf decreased due to chemical desiccation treatments (Sawhney & Singh, 2002). A reduction in chlorophyll content was reported in drought stressed soybean plants by Zhang et al. (2006). The chlorophyll content decreased to a significant level at higher water deficits in maize and wheat plants (Nayyar & Gupta, 2006).

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3.2. Plant Carotenoid Carotenoids are a large class of isoprenoid molecules that are synthesized de novo by all photosynthetic and many non-photosynthetic organisms. They are divided into the hydrocarbon carotenes, such as lycopene and b-carotene or xanthophylls, typified by lutein. Carotenoids are also exploited as colouring agents, furnishing distinctive yellow, orange and red colours to flowers, fruits and roots, where they probably act as attractants to pollinators and for seed dispersal. The colours provided by the pigments are of important agronomical value in many horticultural crops (Bramley, 2002; Niogy et al., 1999; Naik et al., 2003). Carotenoids are essential parts of the pigment protein complexes in thylakoids, and the regulation of carotenogenesis in green tissues must be linked to the formation of chlorophyll, protein, lipid and chloroplast development itself. This highly regulated process is poorly understood. It is known that light and its intensity are involved in the regulation of carotenoid formation in the chloroplast. Although expression of carotenoid genes does occur in etiolated plants, their synthesis is stimulated on transfer to light (Havaux, 1998; Niyogi, 1999; Bramley, 2002).

3.3. Plant Xanthophyll Although the antioxidant defense system is impaired under stressful conditions, plants are able to get rid of excessive energy by thermal dissipation associated with an increase in the concentration of xanthophyll pigments, zeaxanthin, and antheraxanthin, at the expense of violoxanthin in water stressed plants (Alonso et al., 2001). The high proportion of xanthophylls under stress conditions may serve as a protection mechanism in leaves (Reddy et al., 2004). The activation of xanthophyll cycle has also been detected in several other

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plants subjected to drought stress (Foyer, 2000). The xanthophylls cycle may be involved in lowering the yield of triplet chlorophyll formation by pre-emptive quenching of the excited singlet state of chlorophyll (Rontein et al., 2002). Thus, a complex relationship between xanthophylls cycle dependent energy quenching and formation of AOS exists in photosynthetic systems of plants under drought stress (Reddy et al., 2004).

3.4. Plant Protein Mostly there was a significant reduction in protein content under stress due to the increase in proline contents. The reduction in protein content in the chilling stressed plants was correlated with increased proline accumulation (Chen et al., 1999). This may be due to the hydrolysis of protein or the inhibition of protein synthesis by oxidative stress leading to the accumulation of proline (Feng et al., 2003). Protein metabolism has been associated with adaptation of plants to environment changes. Only few reports regarding leaf proteins of sunflower are available. Rodriguez et al. (2002) reported a decrease in leaf soluble proteins in sunflower due to water stress. In contrast, Rabueri et al. (1989) and Ashraf and Mehmood (1990) reported that a higher degree of drought resistance was associated with higher protein contents. However, the nature of plant species (Terri et al., 1986) and the type of tissues modulate the concentration of soluble proteins under water stress (Irigoyen et al., 1992).

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3.5. Plant Soluble Sugars Sugars are considered to play a major role in osmo-regulation under water stress (Fallon & Phillips, 1988). Water deficit caused an increase in the concentration of soluble sugars in the leaves of alfalfa (Irigoyen et al., 1992). Under water-limited conditions, the breakdown of polysaccharides resulted in higher amount of sugars, which helps in maintenance of turgor. Clifford et al. (1998) revealed that sugars are involved in osmotic adjustment in Ziziphus mauritiana under water-limited environment. In contrast, Patakas et al. (2002) observed nonsignificant differences in sugar contents of water stressed and unstressed grapevine plants.

4. EFFECTS OF WATER DEFICIT ON OSMOLITES AND OSMOREGULATION OF HIGHER PLANTS Many plants and other organisms cope with osmotic stress by synthesizing and accumulating some compatible solutes which are termed as osmoprotectants or osmolytes (Pinhero et al., 2001; Shao et al., 2005, 2006). These compounds are small, electrically neutral molecules, which are non-toxic even at molar concentration (Alonso et al., 2001). The osmolytes that accumulated under water stress in plants include proline, aminoacids, polyamines and quarternary ammonium compounds like glycine betaine (Tamura et al., 2003). Decreasing water supply to crop plants greatly reduces growth. Shortage of water affects many key metabolic and physiological processes in plants. Differences in water relation

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characteristics reflect the differences between the species and lines, and are considered as an indicator of drought resistance or adaptation to drought (Subrado & Turner, 1983; Shao et al., 2006, 2007). Particularly, osmotic adjustment active lowering of osmotic potential in response to drought is the mechanism that significantly contributes towards drought resistance (Blum & Sullivan, 1986; Ludlow & Muchow, 1990; Shao et al., 2006). Water deficit decreases leaf water potential in various sunflower lines (Ashraf & O’Leary, 1996), and these lines differed significantly under water stress. The genotypes with lower water potential were considered to be more tolerant to drought. Angadi & Entz (2002b) suggested that under water stress, dwarf sunflower hybrids showed higher acclimation potential, keeping low water potential than all hybrids. In sunflower, leaf water potential usually ranges from –0.48 to –1.74 Mpa under different agroclimatic conditions (Prasad et al., 1985; Rachidi et al., 1993), although under water deficit, it can drops to below as –3.0 Mpa (Wise et al., 1990). The major mechanism of turgor maintenance is osmotic adjustment, thereby decreasing the leaf osmotic potential. The results of Ashraf and O’Leary (1996) showed a decrease in leaf osmotic potential due to water stress. They were of the view that plants showing less reduction in osmotic potential due to drought are more drought-tolerant. Chimenti & Hall (1993) have also reported genetic variation for osmotic adjustment in sunflower. Similarly, Angadi & Entz (2002b) reported genotypic variation in sunflower regarding leaf osmotic potential under water stress. They were of the view that dwarf sunflower lines were more drought-tolerant than tall lines, showing less decrease in leaf osmotic potential in response to drought stress. Maury et al. (2002) observed adaptive responses of leaf water parameters to drought that were quite contrasted in sunflower genotypes. They observed decrease in leaf osmotic potential due to water stress. Turgor maintenance plays a very important role in drought tolerance of plants and this may be due to its role in stomatal regulation, and hence photosynthesis (Ludlow et al., 1985). Under water stress, plants lose their turgor to a point of restricting cell expansion, which ultimately reduced growth (Turner, 1986). Sunflower cultivars showing higher turgor potential under water stress showed less decrease in yield (Angadi & Entz, 2002). However, some evidences indicated that drought tolerance was not associated with leaf turgor potential (Cortes & Sinchair, 1986; Ashraf & O’Leary, 1996).

4.1. Proline Proline content increases in a large variety of plants under stress, up to 100 times the normal level (Barnett & Naylor, 1966), which makes up to 80 percent of the total amino acid pool. Proline was known to accumulate in plants under water stress (Hsaio, 1973). Proline accumulation was maximum at flowering stage and minimum at vegetative stage. Proline content is effective in increasing osmotic status of the plant. The accumulation of proline increased when water stress was followed by simultaneous increase in leaf water potential in chickpea (Gupta et al., 2000). Proline is also regarded as a source of energy, carbon, and nitrogen for the recovering tissues (Singh et al., 1973b; Blum & Ebercon, 1976). Proline was more readily accumulating in the stem (including sheaths) and roots than in the leaves of water stressed wheat plants. Roots are considered as net proline importers (Oakes, 1996; Singh et al., 1973a). Role of proline as an energy, carbon and nitrogen source

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enhances tissue recovery on the relief of stress in sorghum (Blum & Ebercon, 1976) and barley (Singh et al., 1973a). Proline is also known to be involved in reducing the photodamage in the thylakoid membranes by scavenging and/or reducing the production of O2. Proline accumulation in plants is caused, not only by the activation of proline biosynthesis, but also by the inactivation of proline degradation, there by resulting in a decrease in the level of accumulated proline in rehydrated plants (Bohnert & Jensen, 1996). Proline acts as a free radical scavenger and may be more important in overcoming stress than in acting as a simple osmolyte (Reddy et al., 2004). The accumulation of proline under abiotic stress conditions accounts for few millimolar concentrations depending on the species and the extent of stress (Delauney & Verma, 1993; Bohnert & Jensen, 1996; Shao et al., 2007). The accumulation of free proline in response to osmotic stress is known to be regulated by a rate-limiting enzyme P5CS in higher plants and antisense transgenics of Arabidopsis with P5CS cDNA showed morphological alterations in leaves that were hypersensitive to osmotic stress (Nanjo, 1999). In these plants, proline deficiency specifically affected structural proteins of cell walls, suggesting that proline is not only an osmoregulator in osmotolerance and morphogenesis in plant (Reddy et al., 2004). Proline accumulation in response to water deficit was higher at vegetative stages in sorghum (Yadav et al., 2005), bell pepper (Amarjit K. Nath et al., 2005), Gossypium hirsutum (Ronde et al, 1999), wheat (Demir, 2000; Hamada, 2000) and Cyamopsis tetragonoloba (Shubhra et al., 2003). The NaCl treatment also increases the proline content in Cicer arietinum (Pandy & Ganapathy, 1985), Raphanus sativus (Muthukumarasamy et al., 2000), rice (Lin et al., 2002) and Peanut (Girija et al., 2002). Proline is known to be involved in reducing photodamage in the thylakoid membranes by scavenging and or reducing the production of O2 (Reddy et al., 2004). Proline accumulation in plants is caused, not only by the activation of proline biosynthesis, but also by the inactivation of proline degradation, thereby resulting in a decrease in the level of accumulated proline in rehydrated plants (Girija et al., 2002). It can also be inferred that proline acts as a free radical scavenger and may be more impacting in overcoming stress than in acting as a simple osmolytes (Bohnert & Jenson., 1996). Such studies open a new avenue of research for metabolic engineering in several agriculturally important crop plants for drought resistance (Kavikishor et al., 2005). Proline concentrations increase many-fold with reduced leaf water potentials and at this stage photosynthesis is known to be quite reduced (Morot-Guadry et al., 2001). A more common explanation for the accumulation of proline is that it confers advantages by protecting membranes and proteins when RWC decreases (Lawlor & Cornic, 2002). Separately induced dark chilling and drought stress as well as simultaneously induced dark chilling and drought stress resulted in a sharp rising of proline content in soybean plants (Heerden & Kruger, 2002). Free proline accumulation is a common response to the imposition of a wide variety of biotic and abiotic stresses including drought (Heerden & Devilliers, 1996) and chilling (Naidu et al., 1991). Shao et al. (2006a) reported significant variations among proline content in ten wheat genotypes under water deficit stress. Accumulation of proline under chemically applied decication stress in wheat was reported by Sawhney & Sinh (2002). Wheat genotypes responded differently, according to the soil water thresholds, in case of osmotic adjustment (Shao et al., 2006b), at different growth periods. A significant enhancement in proline content with concomitant increase in antioxidant enzymes

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and soluble sugars was reported in different genotypes of Radix astragali at seedling stage (Tan et al., 2006). Chilling stress increased the proline accumulation in cucumber plants (Feng et al., 2003). Increased proline content was met with water deficit stress in soybean, and this was further enhanced by the addition of uniconazole (Zhang et al., 2006). The proline content is maximum in soybean plants under drought stress and altered due to AM symbiosis (Porcel, 2004). Proline, an important compatible osmolytes that stabilizes membranes and protein structure, is normally produced in higher plants in response to environmental stresses (Rhodes et al., 1999; Ozturk & Demir, 2002). It usually accumulates in cytosol and helps the plants to combat abiotic stresses by a process known as osmotic adjustment (Ketchum et al., 1991; Voetberg & Sharp, 1991). Evidences suggest that enhanced proline production, in response to salt stress or drought, may have a role in tolerance to these stresses (Szegletes et al., 2000; Kong et al., 2001; Aspinall & Paleg, 1981; Hsu et al., 2003; Shao et al., 2006, 2007). The physiological significance of stress- induced accumulation of proline is controversial because some investigators have obtained contrasting results regarding the role in stress tolerance of plants (Brock, 1981; Dix & Pearce, 1981). Moreover, the direct evidence for its role in stress tolerance is tenuous (Hanson et al., 1979; Naidu et al., 1998). The increase in proline under abiotic stresses is related to a decrease in leaf water potential (Patil et al., 1984). Genotypic differences regarding proline accumulation under stressful environment is also well documented for different corps (Sivaramakrishnan et al., 1988; Almansouri et al., 1999). Drought tolerant genotypes accumulate greater proline; hence, proline accumulation could be used as selection criterion for stress resistant genotypes (Ashraf & Haris, 2004; Shao et al., 2007). However, it is assumed that proline in plants accumulation is not an adaptive response but only a symptom of stress (Hanson, 1980; Lutts et al., 1999).

4.2. Free Amino Acids Amino acids and other soluble nitrogenous compounds play an essential role in plant metabolism being the primary product of inorganic nitrogen assimilation and precursors of protein and nucleic acids. Because of the importance of soluble nitrogenous compounds, there has been much interest in the influence of environmental stress on their metabolism. A common response of plants to environmental stress is an accumulation of amino acids (Aspinall & Paleg, 1981). The accumulation of total soluble sugar and free amino acids under stress at all the growth stages indicates the possibility of their involvement in osmotic adjustment (Yadav et al., 2005). Osmotic adjustment is one of the important mechanisms, which alleviates some of the detrimental effects of water stress (Morgan, 1984). It has been identified as an important criterion of yield stability and drought tolerance in several crops including sorghum (Santamaria et al., 1990; Ludlow et al., 1990; Morgan, 1995; Chimenti et al., 2002). Free amino acid accumulation is more important accounting for most of the changes in osmotic potential in sorghum (Yadav et al., 2005). Significantly higher accumulation of free amino acids content exists in soyabean (Fututoku & Yamada, 1981), wheat (Munns et al., 1979; Hamada, 2000), drum wheat (Morgan et al., 1986), Olive (Anjuthakur et al., 1998),

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Coconut (Kasturibai & Rajagopal, 2000), groundnut (Asha & Rao, 2002), Oryza sativa (Hsu & Kao, 2003) and bell pepper (Nath et al., 2005). Amino acids play essential roles in plant metabolic processes, being the primary products of inorganic nitrogen assimilation and precursors of proteins and nucleic acids. Some studies have shown that accumulation of amino acids helps plants to overcome water deficit conditions, possibly through osmotic adjustment (Greenway & Munns, 1980). Drought stress increases amino acid accumulation in crop plants (Ranieri et al., 1980). Amino acids accumulation plays a very important role in drought tolerance, probably through osmotic adjustment in different plant species, such as, Morus alba (Ramanjulu & Sudhakar, 1996) and Brassica napus (Good & Zaplachinski, 1994). However, there are some contrasting reports (Patakas et al., 2002) indicating no significant increase in total free amino acids under water stress.

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4.3. Glycine Betaine Betaines are known to be one of the major osmoregulating compounds, forming inner salt with quaternary ammonium groups and a carboxyl group. Among them glycine betaine is the most familiar and widespread in plants and bacteria. Accumulation of glycine betaine occurs in some, but not in all higher plants, and most of the glycine betaine is synthesized in chloroplasts by two enzymes, namely choline monoxygenage (CMO) and betaine aldehydedehydrogenase responsible for glycine betaine synthesis chloroplastically. Glycine betaine synthesis can be induced by both drought and salt stress by over expression of CMO, and betain aldehyde dehydrogenase in barley (Nakamura et al., 2001) stress tolerance in plants (Jun et al., 2000). The accumulation of glycine betaine might serve as an intercellular osmoticum of glycine betaine and could be closely correlated with the elevation of osmotic pressure as in Spartina X townsendii (Storey and Wyn-Jones, 1978). Glycine betaine may maintain the osmoticum, provided that the basal metabolism of the plant can sustain a high rate of synthesis of these compounds to facilitate osmotic adjustment for tolerance to water stress (Kavikishore et al., 1995). Glycine betaine has been shown to protect enzymes and membranes and also to stabilize PSII protein pigment complexes under stressful conditions (Papageorgiou and Morata, 1995). A taxonomically restricted range of species accumulates glycine betaine. In higher plants it is synthesized from choline via betaine aldehyde using choline monooxygenase (BALDH) in chloroplast (Rathinasabapathi et al., 1997). Glycine betaine also accumulates in Arabidopsis (Alia et al., 1999). The NaCl stress increased the glycine betaine content in Raphanus sativus (Muthukumarasamy et al., 2000). Accumulation of glycine betaine occurs in some plants during drought stress. Glycine betaine synthesis can be induced by both drought and salt stress by over expression of betaine aldehyde dehydrogenase (Nakamura et al., 2001). The increased concentration of glycine betaine under drought stress situations cleanly suggest that this osmolyte has an important role in protecting plant cell mechanism under condition of drought. A physiological role of glycine betaine in alleviating osmotic stress was proposed based on accumulation of glycine betaine in plants subjected to drought (Jun et al., 2000). Glycine betaine has been shown to

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protect enzymes and membranes and al so to stabilize PSII protein pigment complexes under stressful conditions (Papageorgiou and Morata, 1995). Glycine betaine is considered to be one of the most abundant quaternary ammonium compounds produced in higher plants under stressful environment (Mansour, 2002; Mohanty et al., 2002; Yang et al., 2003). In higher plants, it is synthesized in chloroplast via a two-step oxidation of choline catalyzed by choline monooxygenase and betaine aldehyde dehydrogenase (Rhodes and Hanson, 1993). In the first step, choline is converted to the hydrate from, betaine aldehyde by ferredoxin dependent choline monooxygenase (Lerma et al., 1988; Broquisse et al., 1989). The second step is the conversion of betaine aldehyde to glycinebetaine catalyzed by a pyridine nucleotide-dependent betaine aldehyde dehydrogenase (Arakawa et al., 1990; Rhodes and Hanson, 1993). The level of glycinebetaine biosynthesis is dependent upon the nature and severity of environmental stresses (Hanson and Wise, 1982; Grieve and Mass, 1984; Yang et al., 2003). Enhanced glycinebetaine synthesis under dehydration stress is accompanied by a higher rate of choline synthesis from serine via ethanolamine (Rhodes and Hanson, 1993), which is then converted into glycinebetaine.

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4.4. Proline Metabolizing Enzymes The proline metabolism was discussed from time to time by several workers (Hayzer and Leisinger, 1980; Dierks Ventling and Tonelli, 1982). Many plants responded to osmotic stress by accumulating high concentration of proline mainly as a result of increased proline biosynthesis (Stewart, 1981; Le Rudulier et al., 1984). Proline biosynthetic pathway in higher plants like soybean and moth bean (Vigna aconitifolia) has been well characterized (Delauney and Verma, 1990; Hu et al., 1992). The pathway of proline biosynthesis starts with glutamic acid. The glutamic acid is converted into glutamic acid γ-semialdehyde by the enzyme complex called pyrroline-5carboxylate synthetase (P5CS). The glutamic acid γ-semialdehyde is converted into pyrroline5 carboxylic acid (P5C) by non-enzymatic cyclization. P-5-C is converted into proline, by the enzyme Δ1-pyrroline-5-carboxylate reductase (Treichel, 1986). The regulation of proline synthesis is probably controlled by the activity of P-5-C synthetase (Boggess et al., 1976). The two enzymes i.e., γ-glutamylkinase and γ-glutamyl phosphate reductase,are regarded as an enzyme complex called P-5-C synthetase because the resulting product glutamic γsemialdehyde (GSA) is non-enzymatically converted to Δ1 pyrroline-5-carboxylate (P5C) (Treichel, 1986).

4. 4.1. Proline Oxidase The typical first response of all living organisms to water deficit is osmotic adjustment. To counter with drought stress, many plants increase the osmotic potential of their cells by synthesizing and accumulating compatible osmolytes such as proline, and for this, the main regulating enzyme is proline oxidase (PROX) (Porcel et al., 2004). A Sharp reduction in proline oxidation was observed under water stress in bean (Flowers and Hanson, 1969) and Zea mays (Sells and Koeppe, 1981). Proline oxidase converts proline to glutamate. Thus this enzyme also influences the level of free proline. The Δ1 pyrroline-5-carboxylate synthetase is the rate-limiting enzyme in prolien biosynthesis in plants and is subjected to feedback

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inhibition by proline. It has been suggested that the feedback regulation of P5CS is lost in plants under stress conditions (Hong et al., 2000).

4.4.2. γ-Glutamyl Kinase γ-glutamyl kinase is an important regulating enzyme in the synthesis of proline. The induction of proline accumulation may be due to an activation of proline synthesis through glutamate pathway involving γ-glutamyl kinase glutamyl phosphate reductase and Δ-pyroline -5- carboxylate reductase activities (Girija et al., 2002). Variation in γ-glutamyl kinase activities was reported in tomato in different physiological regions (Fugita et al., 2003). The first step of proline biosynthesis is catalyzed by γ-glutamyl kinase. γ-glutamyl kinase belongs to a family of amino acid kinase, and a predicted three-dimensional model of this enzyme was constructed on the basis of the crystal structures of three related kinases (Fujita et al., 2003). Plants have two proline biosynthetic pathways the glutamate pathway and orinithine pathway, with the former appearing to play a predominant role under osmotic stress (Rhodes, 1987). In the glutamate pathway, glutamate is converted by γ-glutamyl phosphate reductase to γ-glutamyl semialdehyde. This product cyclizes spontaneously to (P5C) Δ1-pyrroline-5carboxylate, which is reduced by NADPH to proline by Δ1-pyrroline-5-carboxylate reductase (Fujita et al., 2003). The γ-glutamyl kinase activity higher in NaCl-stressed radish (Muthukumarasamy et al., 2000).

5. EFFECTS OF WATER DEFICIT ON NON-ENZYMATIC ANTIOXIDANTS OG HIGHER PLANTS

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5.1. α- Tocopherol α-tocopherol, found in green parts of plants scavenges lipid peroxy radicals through the concerted action of other antioxidants (Munne-Bosch and Alegre, 2002). Zhang and Schmidt (2000) reported a two fold increase in α-tocopherol in turf grass under water stress. α – Tocopherols interact with the polyunsaturated acyl groups of lipids, stabilize membranes, and scavenge and quench various reactive oxygen species (ROS) and lipid soluble byproducts of oxidative stress (Brigelius – Flohe and Traber, 1999; Wang and Quinn, 2000). Synthesis of low-molecular-weight antioxidants, such as α -tocopherol, has been reported in droughtstressed plants (Munne-Bosch and Alegre, 2002). Oxidative stress activates the expression of genes responsible for the synthesis of tocopherols in plants (Falk et al., 2002; Sandorf and Hollander-Czytko, 2002). Antioxidants including α-tocopherol and ascorbic acid have been reported to increase following triazole treatment in tomato and these may have a role in protecting membranes from oxidative damage, thus contributing to chilling tolerance (Senaratna et al., 1988). Photosynthetic apparatus and membrane could be affected by water stress. Alpha-tocopherol is a lipid-soluble antioxidant associated with biological membrane of cells, especially the membrane of photosynthetic apparatus (Lawlor, 1995). Burger et al. (1951) noted that tocopherol content of soybean leaves was increased as the amount of rainfall decreased. This is consistent with the reports of Tanaka et al. (1990), who showed that subjecting spinach to water deficit increased the content of -tocopherol in the leaves. Based on the studies of 10

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different grass species under water stress, Price and Hendry (1989) found that drought stress led to an increase of 1 to 3-fold of -tocopherol concentration in 9 out of 10 species. They pointed out that the species with a high tolerance of stress are defended through tocopherol. Moreover, highly significant correlations were observed between stress tolerance and tocopherol concentration (the precursor of α-tocopherol; Spearmans rank correlation coefficient r = 0.731).

5.2. Ascorbic Acid A continuous oxidative assault on plants during drought stress has led to the presence of an arsenal enzymatic and non-enzymatic plant antioxidant defenses to counter the phenomenon of oxidative stress in plants (Reddy et al., 2004). The ascorbic acid (AA) is an important antioxidant, which reacts not only with H2O2 but also with O2-, OH and lipid hydroperoxidases (Munne Bosch and Algere, 2003). Water stress resulted in significant increase in antioxidant AA concentration in turf grass (Zhang and Schmidt, 2000). Ascorbic acid showed a reduction under drought stress in maize and wheat, suggesting its vital involvement in deciding the oxidative response (Nayyar and Gupta, 2006). Zhang and Kirkam (1994) reported a decrease in the level of antioxidants including ascorbic acid with increase in stress intensity in wheat. Ascorbic acid can also directly scavenge 1O2, O-2 and •OH and regenerate tocopherol from tocopheroxyl radicals, thus providing membrane protection (Thomas et al., 1992).

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5.3. Reduced Glutathione Glutathione is a tripeptide (α-glutamyl cysteinylglycine), which has been detected virtually in all cell compartments such as cytosol, chloroplasts, endoplasmic reticulum, vacuoles and mitochondria (Noctor and Foyer, 1998). Glutathione is the major source of nonprotein thiols in most plant cells. This reactivity along with the relative stability and high water solubility of GSH makes it an ideal biochemical to protect plants against stress including oxidative stress, heavy metals and certain exogenous and endogenous organic chemicals (Noctor et al., 2002). Reduced glutathione (GSH) acts as an antioxidant and is involved directly in the reduction of most active oxygen radicals generated due to stress. Gopal and Verma (2001) reported that glutathione, an antioxidant helped to withstand oxidative stress in transgenic lines of tobacco.

6. EFFECTS OF WATER DEFICIT ON ANTIOXIDANT ENZYMES OF HIGHER PLANTS The degree to which the activities of antioxidant enzymes and the amount of antioxidant increase under drought stress will be extremely variable among several plant species and even between two cultivars of the same species. The level of response depends on the species, the

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development and metabolic state of the plant, as well as the duration and intensity of the stress. Many stress situations cause an increase in the total foliar antioxidant activity (Pastori et al., 2000). The different antioxidant enzymes in plant cells that are subjected to drought stress (Reddy et al., 2004; Shao et al.,2008b). Acclimation of plants to changing environmental conditions such as drought stress is essential for survival and growth. Drought stress causes the production of reactive oxygen radicals or species (ROS). The ROS are responsible for most of the oxidative damage in biological systems (Reddy et al., 2004). Mechanisms of ROS detoxification exist in all plants and can be categorized as enzymatic (SOD, APX, POX, GR etc.) and non enzymatic (Asocrbic acid, flavanones, anthocyanins etc.). The level of response depends on the species, the development and the metabolic state of plant, as well as duration and intensity of stress. Many stress situations cause an increase in the total foliar antioxidant activity (Pastori et al., 2000). It is also known that plant resist the stress-induced production of active oxygen species (AOS) by increasing components of their defensive system (Del Rio et al., 1991; Salin, 1991; Foyer et al., 1994). Plant cells are normally protected against such effect by a complex antioxidant system as non-enzymic and enzymic antioxidants (Winston, 1990; Smirnoff, 1993). A large number of studies deal with various oxidative stress factors in plants, and describe how exposed plant adjust their detoxifying enzyme activities (Tsang et al.,1991; Bowler et al.,1991; Sgherri et al.,1993; McKersie et al., 1993 ; Herouart et al., 1994; Van Camp et al., 1996). Key enzymes inolved in the detoxification of ROS (reactive oxygen species) are namely superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), ascorbate peroxidase (APX) and other enzymes implicated in the Halliwell and Asada cycle (Ascorbate–Glutathione Pathway). Under stress condition an enhanced activity of almost all these enzymes has been reported (Zaka et al., 2002; Jaleel et al., 2006a, 2007a, 2007b).SOD, CAT and POD are important antioxidant systems antioxidant systems and superoxide

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dismutase catalyses the dismutation of O2 to H2O2 and O2, while catalase and peroxidase scavenge H2O2 (Foyer et al., 1994). Feng et al. (2003) showed that chilling could weaken the enzymatic antioxidant system of cucumber seedlings and induce an increase in H2O2 level, thereby exposing them to oxidative stress. Other authors observed similar effects in rice (Huang, 2000; Liang and Wang, 2001; Wang and Liang, 1995).

6.1. Superoxide Dismutase (SOD) SOD is one of the ubiquilous enzymes in aerobic organisms and plays a key role in cellular defense mechanisms against reactive oxygen species. Its activity modulates the reactive amounts of O2− and H2O2, the two Haber-weiss reaction substrates, and decreases the risk of OH radical formation, which is highly reactive and may cause severe damage to membrane, protein and DNA (Bowler et al., 1992). Generation of superoxide is promoted in drought stressed plant cells (Price et al., 1989). SOD activity increased under drought stress in Oryza sativa (Reddy et al., 1998), Euphorbia esula (Davis and Swanson, 2001), maize (Pastori et al., 2000; Jiang and Zhang, 2002), Cassia angustifolia (Agarwal and Pandey, 2003) and wheat (Singh and Usha, 2003; Shao et al., 2005); rice (Wang et al., 2005), P. acutifolius (Turkan et al., 2005) and the SOD activity was higher under salinity stress in C. roseus (Misra and Gupta, 2005; Jaleel et al.,

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2007c). While subjecting to water deficit stress to higher plants, SOD activity was increased in higher plants (Reddy et al., 2004; Manivannan et al., 2007a). SODs, discovered by McCord and Fridovich in1969, are ubiquitous metalloenzymes that catalyze the disproportionation of superoxide radical anions to dioxygen and hydrogen peroxide. SOD is the most efficient scavengers of the superoxide anion and an essential component of the ascorbate-glutathione cycle (Bannister et al., 1987; Foster and Hess, 1982; Beyer et al., 1991; Halliwell, 1974; Harper and Harvey, 1978; Monk et al., 1989; Nakano et al., 1980) for the detoxification of toxic oxygen species. Higher plants have SODs containing Cu and Zn, Fe, or Mn as prosthetic metals. Copper/ Zn-SOD is found in both chloroplasts and cytosols, whereas Mn-SOD is found in the matrix of mitochondria. Iron-SOD has been reported in chloroplasts, mitochondria, and peroxisomes of petals in a few plants (Bowler et al., 1992). SOD has been one of the most widely studied enzymes in the antioxidant system (Bowler, 1991, 1994). The importance of SOD for aerobic growth has been established by demonstration that the SOD-deficient mutant of E. coli (Carlioz and Tonati, 1986) is hypersensitive to oxygen. Recent research indicates that tobacco and alfalfa expressing high levels of Mn-SOD targeted to chloroplasts or mitochondria are more tolerant to paraquat and freezing, respectively (Bowler et al., 1991; Mckersie et al., 1994). Several researchers have indicated that SODs play an important role in water stress tolerance of plants (Bowler, 1992). Increased SOD activity was reported in Radix astragali under water deficit stress, which varied in three different genotypes (Tan et al., 2006). Chilling stress has significant effect in the enhancement of SOD activity in cucumber seedlings (Feng et al., 2003). The increase in SOD activity under drought stress was about 25% in soybean plants (Zhang et al., 2006). The amount of double SOD activity was noted in water stressed citrus plants when compared to well water control plants during seedling stage (Wu et al., 2006). The combined action of superoxide dismutase and catalyse abate the formation of the most toxic and highly reactive oxidant, the hydroxyl radical (OH), which can react indiscriminately with all macromolecules. Important function of superoxide dismutase is to prevent radical mediated chain oxidation of reduced glutathione, thereby enabling reduced glutathione to act physiologically as a free radical scavenger without concomitant oxidative stress to the cell. The combination of superoxide dismutase and reduced glutathione plays a significant role in intracellular antioxidant defence (Asada, 1999 b).

6.2. Peroxidase (POX) POX plays a role in decreasing H2O2 content accumulation, eliminating MDA from resulting cell peroxidation of membrane lipids and maintaining cell membrane integrity. Radix astragali plants under water deficit stress showed an enhancement in POX activity irrespective of different genotypes (Tan et al., 2006). Increased POX activity was reported in chilling stress cucumber seedlings by (Feng et al., 2003). Increased POX activity was reported in low temperature stressed wheat seedlings (Berova et al., 2002). Water deficit stress increased the POX activity in soybean plants (Zhang et al., 2006), which is further increased by uniconazole treatment. POX is involved in various metabolic steps such as auxin catabolism (Normanly et al., 1995), the formation of iso di-try bridges in the cross-linking of cell wall proteins (Schnabelrauch et al., 1996), the cross-linking of pectins by diferulic bridges in tobacco

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(Amaya et al., 1999) and the oxidation of cinnamyl alcohols prior to their polymerization during lignin and suberin formation (Roberts et al., 1988; Whetten et al., 1998).

6.3. Ascorbate Peroxidase (APX) APX exists as iso-enzymes and plays an important role in the metabolism of H2O2 in higher plants (Shigeoka et al., 2002). APX isoenzymes are critical components that prevent oxidative stress in photosynthetic organisms. Additionally, recent studies on the response of APX expression to some stress conditions and pathogen attack indicate the importance of APX activity in controlling the H2O2 concentration in intercellular signalling. APX activity increased under drought stress in Euphorbia escula (Davis and Swanson, 2001), Zea mays (Jiang and Zhang, 2002), wheat (Dalmia and Sawhney, 2004), P. accutifolius (Turkan et al., 2005) and soybean (Riekert van Heerden and Kruger, 2002). APX reduces H2O2 to water by ascorbate as specific electron donor (Gara et al., 2003). In trifoliate orrange, under water stress, an increased APX activity was no significant variation in APX activity at mild water deficit in maize and wheat (Nayyar and Gupta, 2006). The APX activity increased in soybean under water stress (Heerden and Kruger, 2002). Sofo et al. (2004) observed that leaves of olive trees experiencing severe drought stress showed more APX activity than the roots, which was assigned to chloroplast APX of the leaf tissue.

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6.4. Catalase (CAT) Catalase (CAT) is of high capacity but it is a low-affinity enzyme, which destroys hydrogen peroxide. In Nicotiana plumbaginifolia leaves, the major part of the catalase activity is due to peroxisomal catalase, which deloxifies hydrogen peroxide produced by photorespiration (Nicholas Smirnoff, 1998). Catalase activity increased under drought stress in Oryza sativa (Reddy et al., 1998), maize (Pastori et al., 2000), Zea mays (Jiang and Zhang, 2002), Allium schoenoprasum (Egert and Tevini, 2002) and wheat (Dalmia and Sawhney, 2004; Shao et al., 2005), P. acutifolius (Turkan et al., 2005). An increase in catalase activity was reported in higher plants under drought stress (Reddy et al., 2004). Similar results were found in Lotus cornicutus (Borsani et al., 2001), rice (Wang et al., 2005). Water stress caused an enhancement of CAT activity in both wild and cultivated species of Radix astragli at seedling stage (Tan et al., 2006). A decrease in CAT activity was reported by Feng et al. (2003) in cucumber seedlings under chilling stress. A two-fold increase in CAT activity was met with Poncirus trifoliata plants under water stress (Wu et al., 2006). Nayyar and Gupta (2006) reported foliar CAT activity enhancement under water stress in wheat and maize. CAT are tetrameric heme containing enzymes that catalyse the dismutation of hydrogen peroxide into water and oxygen (Fornazier et al., 2002). The enzyme is abundant in the glyoxisomes of lipid-storing tissues in germinating barley, where it decomposes H2O2 formed during the ß-oxidation of fatty acids (Holtman et al., 1994) and in the peroxisomes of the leaves of C3 plants, where it removes H2O2 produced during photorespiration by the conversion of glycolate into glyoxylate (Kendall et al., 1983; Willekens et al., 1997). This is also due to the fact that there is proliferation of peroxisomes during stress, which might help in scavenging of H2O2 which can diffuse from the cytosol (Lopez-Huertas et al., 2000). A

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third class of catalase is located in vascular tissues and may be involved in protection against environmental stress (Willekens et al., 1994).

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7. CONCLUSIONS AND PERSPECTIVES It is clear that insights into the physiology and molecular biology of drought tolerance in higher plants will enable us to determine which genes could, either singly or in combination, confer some degree of similar tolerance to plants. Drought is one of the major problems facing in world wide agriculture and ecoenvironment. The economic losses from insufficient water supply are major and considerable for a long time and increase in agricultural productivity can be brought about by the production of drought tolerant crops. Improvement of ecoenvironment will be realized finally by making the best use of plant resources at different scales.The study of physiological mechanisms of anti-drought has much work to do. Molecular biology aspects can not substitute for this important part, but can strengthen the research and provide a broad future .It is easy to see that one cell or molecule can not be alive in natural fields and not provide any economic effect for human beings.The combination of molecular biology and plant physiology is the key. Many achievements in biotechnological and traditional breeding are good examples. Although some progresses in terms of the exploration of molecular anti-drought genes have taken place, many problems exist (Figure 3). What is the relationship of mineral elements(in particular,K+, Na+,Ca2+)with root signal transduction(pathways)?Much of former study showed that K+ was little connected with antidrought,but recent research and our results displayed that it was linked with wheat resistance drought. What is the exact soil water stress threshold of individual plant species and their corresponding genotypes?This is of much importance to anti-drought breeding and savingagriculture and precise agriculture under global climate change.What are the details that constitute the network regulatory system of drought, cold ,UV-B ,freezing, acidity ,salty, wounding ,pathogen, senescence, cell death? How is each linked with other parts? What is the (transient) connection among different physiological adaptive regulatory pathways at different levels? What roles do endogenous hormones play in this course? What is the crosstalk among them when abiotic or/and biotic stress happens? The redox state in plants is important, and how is it regulated? What is the relationship with microRNAs? What is the exact role for ABA during plant adaptation to drought stress and its corresponding receptors in biomembrane (Figure 1,2)? Much more needs identification and explanation for this hot topic.A widespread use of data resources for fine gene functions and structure of different plants (species) is from model plants, Arabidopsis thaliana and rice, and how large is the reliability? It is also important to notice the fact that drought is not only controlled by multigenic genes,but also overlapped and interacted with other abiotic stresses such as cold,heat and salt in terms of its mechanisms and phenotypes,which makes drought stress more complicated. No doubt, expanded detecting of plant range is more urgent. So, we think that physiological studies at different scales have much work to do with the increasing atmospheric change. No doubt, the above issues are and will be the greatest challenge in 21st century for plant biologists, agricultural scientists and soil scientists.

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ACKNOWLEDGEMENTS The research in this article is jointly supported by 973 Project of China (2007CB106803), Shao Ming-An’s Innovation Team Group Projects of Education Ministry of China and Northwest SA&F University, the International Cooperative Partner Plan of Chinese Academy of Sciences, and the Cooperative&Instructive Foundation of State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau(10501-HZ)(To Shao HB). The authors apologized for not citing all the authors of original publications because of space limitation.

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Asada, K. Ascorbate peroxidase a hydrogen peroxide scavenging enzyme in plants. Physiol Plant, 1992; 85: 235-41. Asada, K. The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol. 1999b; 50: 601-39. Asada, K. The role of ascorbate peroxidase and monodehydroascorbate reductase in H2O2 scavenging in plants. In : Scandalios J.G. ed. Oxidative stress and the molecular biology of antioxidant defences. Cold Spring Harbor Laboratory Press.1999a, pp.715-735. Asha, S. and Rao, K.N. Effect of simulated waterlogging on the levels of amino acids in groundnut at the time of sowing. Ind J Plant Physiol. 2002; 7: 288-91. Aspinall, D. and Paleg, L.G. Proline accumulation: physiological aspects: In: Paleg L.G. and Aspinall D. (Eds.), Physiology and biochemistry of drought resistance in plants. Academic Press, Sydney, Australia, 1981, pp. 215-228. Babu, V.R. and Rao, D.V.M. Water stress adaptations in the ground nut (Arachis hypogara L.)- foliar characteristics and adaptations to moisture stress. Plant Physiol Biochem. 1983; 10: 64-80. Barnett, N.M and, Naylor, A.W. Plant Physiol. 1996; 41: 1222-30. Bellinger, Y. and Larher, F. Proline accumulation in higher plants: A redox buffer? Life Sci Adv. 1987; 6: 23-7. Berman ME, Dejong TM. Water stress and crop load effects on fruit fresh and dry weights in peach (Prunus persica). Tree Physiol 1996; 16: 859-64. Berova, M., Zlatev, Z. and Stoeva, N. Effect of paclobutrazol on wheat seedlings under low temperature stress. Bul J Plant Physiol. 2002; 28: 75-4. Berry, S.K., Kalra, C.L., Sehgal, R.C., Kulkarni, S.G., Kaur, S., Arora, S.K., and Sharma, B.R. Quality characteristics of seeds of five okra (Abelmoschus esculentus (L). Moench). Cultivars. J Food Sci Tech. 1998;25: 303-5. Bhagsari, A.S., Brown, R.H. and Schepers, J.S. Effect of moisture stress on photosynthesis and some related physiological characteristics in peanuts. Crop Sci. 1976; 16: 712-5. Bhatt, R.K. Seasonal variation in light absorption and transpiration in Prunus,celtis and Grewia. Ind J Forestry, 1990;13: 118-21. Bhatt, R.M. and Srinivasa Rao, N.K. Influence of pod load on response of okra to water stress. Ind J Plant Physiol. 2005; 10: 54-9. Blum, A. Crop response to drought and the interpretation of adaptation. Plant Growth Regul. 1996; 20:135-48. Blum, A. and Ebercon, A. Genotypic responses in sorghum to drought stress. III. Free proline accumulation and drought resistance. Crop Sci. 1976; 16: 428-31. Blum, A. and Arkin, G.F. Sorghum root growth and water use affected by water supply and growth duration. Field Crop Res. 1984;9:131-49. Boggess, S.F., Stewart, C.R., Aspinall, D., and Paleg L.G. 1976. Effect of water stress on proline synthesis from radio active precursors. Plant Physiol. 1976; 58: 398-401. Bohnert, H.J. and Jensen, R.G. Strategies for engineering water stress tolerance in plants. Trends Biotech. 1996;14: 89-97. Bolwell, G.P. Role of active oxygen species and NO in plant defense responses. Cur Opin Plant Biol. 1999; 2: 287-94. Bonan, G.B. The size structure of theoritical plant populations: spatial patterns and neighborhood effects ecology. Ecol. 1988;69: 1721-30.

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Vyas, S.P., B.K. Garg, S. Kathju, and A.N Lahiri.Influence of potassium on water relations, photosynthesis, nitrogen metabolism and yield of cluster bean under soil moisture stress. Ind J Plant Physiol. 2001; 6:30-7. Wang, S.G. and Y. Liang. Protection of 6-benzyladinine on cell membrane system of rice seedlings under chilling stress. J Rice Sci. 1995; 9: 223-9. Wang, X. and P.J. Quinn. The location and function of Vitamin E in membrances (review). Mol Membr Biol. 2000;17: 143-56. Wang, F.Z., Q.B. Wang, S.Y. Kwon, S.S. Kwak, and W.A. Su. Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol. 2005;162: 465-72. Watson, D.J. The physiological basis of variation in yield. Adv Agron. 1952; 4: 101-44. Weber, J.A. and D.M. Gates. Gas exchange in Quercus rubra during a drought: analysis of relation among photosynthesis, transpiration and conductance.Tree Physiol. 1990; 7: 21525. Weigh, M..Evidence for increased sensitivity to nutrient and water stress in a fast-growing hybrid willow compared with a natural willow clone. Tree Physiol. 2001; 21: 1141-48. Weiner, J. Size hierarchies in experimental populations of annual plants. Ecol. 1985; 66: 74352. Wheatley, A.R.D., J.A. Whiteman, J.H. Williams, and S.J. Wheatly. The influence of drought stress on the distribution of insects on four groundnut genotypes grown near Hyderabad. Ind Bull Entol Res. 1989;79: 567-77. Wightman, J.A. and A.S. Wightman. An insect, agronomic and sociological survey of groundnut fields in southern Africa. Agri Ecosystem Environ. 1994; 51: 311-31. Willekens, H., C. Langebartels, C. Tire, M. Vanmontagu, D. Inze, and W. Vancamp. Differential expression of catalase gene in Nicotiana plumbagini folia L. PNAS, 1994;91:10450-54. Willekens, H., D. Inze, M. Van Montagu, and W. Van camp.Catalase in plants. Mol Breeding, 1997; 1: 207-28. Winston, G.W. Physiochemical basis for free radical formation in cells: production and defenses. In stress responses in plants: Adaptation and acclimation mechanisms. Alscher RG and JR Cumming (eds.). Wiley-Liss, Inc. New York, 1990, pp. 57-86. Wright, G.C. and R.C.N. Rao.Genetic variation in water-use efficiency in groundnuts. In: Nigam SN(ed), Groundnut-A global perspective. International Crops Research Institute for the Semi-arid Tropics, Patancheru, India,1992, p.460. Wright, G.C., K.T. Hubick, G.D. Fraquhar, and R.C. Nageswara Rao. Genetic and environmental variation in transpiration efficiency are in correlation with carbon isotope discrimination and specific leaf area in peanut. In: Ehleringer JR, Hall AE, Fraquhar GD(eds), Stable isotope and plant carbon water relations.Academic Press. New York,1993, pp.247-267. Wu, D.X. and G.X. Wang. The dynamics of size inequality in spring wheat populations under semi-arid conditions and its physioecological basis. Acta Ecol Sin. 1999; 19: 254-8. Xin, X.P., G. Wang and S.L. Zhao.Size hierarchy and its genetic analysis in spring wheat population under different water conditions.Acta Phytoecol Sin. 1998; 22: 157-63. Yadav, S.K., N.J. Lakshmi, M. Maheswari, M. Vanaja, and B. Venkateswarlu.Influence of water deficit at vegetative, anthesis and grain filling stages on water relation and grain yield in sorghum. Ind J Plant Physiol. 2005;10:20-24.

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Yamaguchi J, T Iwamoto, S Kida, S Masushige, K Yamada, T Esashi.Tocopherol associated protein is a ligand dependent transcriptional activator. Biochem Biophy Res Comm 2001; 285: 295-9. Yamaguchi, K., H. Mori, and M. Nishimura. A noval isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol. 1995b; 36: 1157-62. Yamaguchi, K., Y. Takeuchi, H. Mori, and M. Nishimura. Development of microbody membrane proteins during the transformation of glyoxysomes to leaf peroxysome in pumpkin cotyledons. Plant Cell Physiol. 1995a; 36: 455-64. Yancy, P.H., M.E. Clark, S.C. Hand, R.D. Bowlus, and G.N. Somero. Living with water stress: evolution of osmolyte systems. Science, 1982; 217:1214-23. Yin, C., X. Wang, B. Duan, J. Luo, and C. Li. Early growth, dry matter allocation and water use efficiency of two Sympatric populus species as affected by water stress. Environ Exp Bot. 2005; 53: 315-22. Zhang, X. and R.E. Schmidt.Hormone containing products impact on antioxidant status of tall fescue and creeping bentgrass subjected to drought. Crop Sci. 2000b; 40 :1344-49. Zhang, X. and R.E. Schmidt.Application of trinexapac-ethyl and propiconazole enhances superoxide dismutase and photochemical activity in creeping bentgrass (Agrostis stoloniferous Var.palustris). J Amer Soc Horti Sci. 2000a; 125: 47-51. Zhang, X., R. Zang and C. Li. Population differences in physiological and morphological adaptations of Populus davidiana seedlings in response to progressive drought stress.Plant Sci. 2004; 166: 791-7. Zhao, H., Zhang, Z.B., Shao, .HB., Xu, P., and M.J. Foulkes.Genetic Correlation and Path Analysis of Transpiration Efficiency for Wheat Flag Leaves. Environ Exp Bot. 2008 (in Press). Zhu, J.K. Salt and drought stress signal transduction in plants.Ann Rev Plant Biol. 2002; 53: 247-73.

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In: New Plant Physiology Research Editor: Robert T. Devane

ISBN 978-1-60741-102-4 © 2009 Nova Science Publishers, Inc.

Chapter 2

PHYSICAL AND CHEMICAL SIGNALS AND THEIR ACTION IN SYSTEMIC RESPONSES OF PLANTS TO LOCAL WOUNDING Vladimíra Hlaváčková* Laboratory of Biophysics, Department of Experimental Physics, Palacký University, tř. Svobody 26, 771 46 Olomouc, Czech Republic

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ABSTRACT Wounding, caused either by physical injury or by herbivore or insect attack, is one of the most severe plant stresses. Higher plants respond to such stress by initiating various defence-related processes, which include accumulation of defence-related proteins, gene expression, stomata movements and changes in respiration and photosynthesis. These processes take place locally, i.e. in the wounded leaf, but many defence responses were detected also in undamaged leaves distal to the site of wounding (systemic response). This finding indicates that a signal moves from the injured tissue to the distant untreated parts of the plant, where it triggers systemic response. Several kinds of chemical and physical signals have been identified in plants responding to local stress. Despite intensive research, there are still many controversial questions about the origin of these long-distance moving signals, their interaction and connection to systemic defence responses. In the following chapter, the main characteristics of physical signals will be discussed together with the mechanism of the generation and propagation of these signals in wounded plants. Methods of electrical signal measurements will be also presented. At the same time, selected chemical signals will be described, with particular focus on the localization of their biosynthesis in plants and their long-distance transport mechanisms after local wounding. An overview of possible interactions between physical (electrical and hydraulic) and chemical (abscisic acid, jasmonic acid, systemin, hydrogen peroxide, ethylene, oligosaccharides, volatiles) signals in long-distance signaling pathways after

*

Email: [email protected], telephone: +420585634179, facsimile: +420585225737

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Vladimíra Hlaváčková local wounding will be given and physiological responses of plants to both physical and chemical wound-induced signals will be outlined.

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1. INTRODUCTION During their life cycle, plants have to cope with numerous environmental factors such as pathogen attack, desiccation stress, changes in temperature, light conditions or wounding. Unlike animals, plants are sessile and cannot usually escape, when they are in danger. Therefore they had to develop effective self-defence related strategies to protect themselves against both biotic (pathogen infection) (Balachandran et al. 1997) and abiotic (wounding, herbivore attack, heat, electrical current) (Wildon et al. 1992, Peña-Cortés and Willmitzer 1995, Peña-Cortés et al. 1995, De Bruxelles and Roberts 2001, León et al. 2001, Schilmiller and Howe 2005) stresses. Over the past 30 years it has been revealed that the plant defence reactions are very complex and that they are tightly interconnected via a remarkable system of intercellular signals. At the same time, signaling pathways are indispensable for the regulation and coordination of stress responses in different parts of the plant. Plant experiencing a local stress responds not only locally, i.e. directly at the site of injury, but defence responses can be detected also in undamaged tissues far from the site of damage. Such defence reactions are referred to as “systemic”. Local and systemic plant reactions are often functionally connected, as defence processes generated locally are usually faster and trigger slower long-distance signaling pathways (i.e. systemic response). Recent research has revealed that the plant signaling pathways are nearly as complex as those of animals. At the molecular level, plants have many components found in animal neuronal system. Obviously, plants do not have nerves, but an amazing number of the neuronal cell infrastructure components are present indeed (e.g. action potentials, voltagegated ion channels, neurotransmitters, vesicle-mediated transport of auxin in specialized vascular tissues, cellular motors, Baluška et al. 2006, Baluška et al. 2005, Trewavas 2003). Having in mind these striking similarities between plant and animal kingdoms, scientists have recently established a new field of plant physiology, so-called “Plant Neurobiology” (Brenner et al. 2006). The main goal of this newly established research field is to elucidate the structure of the information network that exists within plants. One part of “Plant Neurobiology” research is also focused on the action of systemic signals, taking into account the combined molecular, chemical and electrical components of intercellular plant signaling. Wounding, caused both by physical injury and herbivore or insect attack, is one of the most severe environmental stresses that plants encounter during their life. Among the other responses of plants to external stimuli, wound response is thought to be one of the most rapid. Fast (minutes to hours) responses to injurious factors have been detected locally as well as systemically at the tissue-, cellular- and molecular- levels in various plants (Herde et al. 1996, Baldwin et al. 1997, Rakwal et al. 2002, Koziolek et al. 2004). These findings suggest that a signal moves from the damaged tissue to the distant undamaged part of the plants and leads to systemic changes. Several kinds of chemical (Peña-Cortés et al. 1995, León et al. 2001) and physical (Stanković et al. 1998) signals, as well as their combination (Malone 1996), have been proposed to be involved in the response of plants to local wounding. In this review, I summarize the present state of knowledge about the origin of the longdistance moving physical (electrical, hydraulic) and selected chemical (mainly JA, ABA)

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signals. I am going to discuss their interaction and connection to systemic changes as well as possible mechanisms whereby they mediate the systemic response of plants to local wounding.

2. PHYSICAL SIGNALS

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2.1. Hydraulic Signals Hydraulic signals in plants are self-propagating pressure waves spreading in vascular bundles. I will focus on hydraulic signals travelling through the plant xylem and participating in systemic physiological responses. Following changes are interpreted as reflecting wound-induced hydraulic signals. Malone and Stanković (1991) showed that a rapid (within seconds) systemic turgor pressure increases in epidermal cells of wheat leaves followed localized wounding by heat. Displacement transducers were used to demonstrate that localized scorching caused also a rapid and systemic increase in leaf thickness in seedlings of wheat (Malone 1992). A small transient decrease in diameter starting a few seconds after the remote burning, followed by a major increase was demonstrated in Vitis vinifera stem (Mancuso 1999). An interesting question is how does the hydraulic signal arise in wounded plants. One attractive hypothesis was pronounced by Malone (1993), who suggests that localized wounding initiates hydraulic signals by destroying cell membranes (Malone 1993). According to this hypothesis, water, previously constrained within cells by osmotic gradients, is released into the apoplast where it becomes available to the nearest xylem. The water in the xylem is normally under negative tension and therefore the available sap will be immediately drawn into the xylem. This will locally increase the xylem tension and the xylem pressure change will propagate basipetally and acropetally throughout the shoot as a hydraulic signal. The increase in xylem pressure connected with the hydraulic surge is sensed by membrane-located mechano-sensitive channels or pumps of surrounding living cells, triggering the cell response (Malone and Stanković 1991, Stanković et al. 1997, Mancuso 1999). The mass flow (“hydraulic dispersal”) from the wounded site is another component of the hydraulic signal. It generally lasts for several minutes, because all cells of the shoot are in hydraulic equilibrium with their nearest xylem. When xylem pressure is boosted systemically by a localized wound, all cells of the shoot will tend to reach the new equilibrium by drawing water from their local xylem. This will lead to the reduction of xylem pressure throughout the healthy tissue, which will further promote the entry of water from the wounded tissue into the xylem. This continues until all water released at the wound site is exhausted. Shortly after the wounding, when fluid is freely available to the xylem at the wounded site, this site will replace the root medium as the most accessible source of water for the plant transpiration. Thus, transiently, the transpiration from healthy leaves will tend to draw water also basipetally down the petiole of the wounded leaf, and possibly also down the stem towards the nodes of more basal leaves. Thus, the flow can be directed in both acropetal and basipetal direction in the stem and can carry fluid and solutes which have entered the xylem of the stem shortly after wounding (Malone 1993, 1994c). Malone (1993) concluded that the woundinduced mass flow can transport solutes extensively and rapidly from the wounded site. The

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mass flow appears to be sufficiently fast (10 mm s-1) to distribute elicitors throughout the plant within the shortest times observed for systemic wound-induction of proteinase inhibitor genes (within minutes, Herde et al. 1998a). Elicitors carried by the mass flow can be sensed by ligand-modulated ion channels of target cells, which was suggested as the mechanism underlying the systemic signaling of wounding in tomato (Malone 1993) and Mimosa (Malone 1994c) plants. Thus, it still remains to be elucidated if chemical (elicitors), physical (pressure surge) or both hydraulic components cooperate in triggering the systemic plant response.

2.2. Electrical Signals The term “electrical signal” is usually used for the description of electrical activity in plants that involves changes in membrane potential. Basically, there are two types of longdistance electrical signals in plants - action potentials (AP) and variation potentials (VP).

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2.2.1. Action Potential Understanding the action potentials (APs) and their role in long-distance electrical signaling is based on detailed studies of animal systems, the classic example being the giant nerve axon of the squid. For electrophysiology of plants, giant cells (1mm in diameter and several cm long) of various species of Charophyta are the equivalent of the giant nerve axon of the squid. The main characteristics of action potentials in the Charophyta, carnivorous and seismonastic plants have already been reviewed several decades ago (Sibaoka 1966, 1969, Pickard 1973, Thain and Wildon 1992, Beilby 2007). Later, the ion mechanism and further characteristics of APs were studied also in other higher plants like tomato (van Sambeek and Pickard 1976b), sunflower (Davies et al. 1991, Zawadski et al. 1991), potato (Fisahn et al. 2004). 2.2.1.1. Generation of Action Potential In resting cells of higher plants the cytoplasm is electrically negative compared to the extracellular medium (membrane potential values in the range -100 to -200 mV, Findlay and Hope 1976). AP is initiated by calcium influx into the cytosol (Figure 1a), followed by the efflux of chloride ions via Ca2+-activated anion channels (Figure 1b) (Trebacz et al. 2006). This results in lowering the membrane potential difference and the plasma membrane becomes depolarized. If the membrane potential difference drops below a certain threshold value, rapid and large depolarization of the membrane is triggered that propagates through the whole cell (Figure 1b) – action potential. After the generation of action potential the membrane enters a refractory period, when its further excitation is impossible (Zawadzki et al. 1991). The repolarization of the membrane occurs after closing of Cl- channels and opening of voltage-gated potassium channels, which allow K+ efflux from the cytosol (Figure 1c). At the same time, Ca2+ ions in cytoplasm evoke an opening of ion channels located in the vacuolar membrane and Cl- is transported into cytoplasm (Figure 1c). In the last phase, calcium pumps in plasmatic membrane translocate the redundant Ca2+ ions back to the apoplast (Figure 1c). The cytoplasm becomes more negative and membrane potential difference is restored to its initial value.

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Figure 1. Simplified model of ion mechanism of action potential generation in plants. For details see the text.

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2.2.1.2. Propagation And Characteristics Of Plant Action Potential In plants APs appear typically after non-damaging stimuli (e.g. electrical stimuli, light/dark transitions, brief cooling and pollination) and are characterized by a constant amplitude, a constant propagation rate and a regular shape (Stanković et al. 1998, Dziubinska et al. 2001). They fulfil classical electrophysiological laws as all-or-none law, strengthduration relation and the presence of refractory periods (Zawadski et al. 1991). APs are self-propagated electrical signals mediated through voltage-gated channels and can spread over the whole plant. Fast AP transmission within short distances is mediated by plasmodesmata. This was observed for example in carnivorous plants, where numerous plasmodesmata ensure connection between the cells of the sensory hair and cells responsible for trap closure (Iijima and Sibaoka 1982). Cells connected with plasmodesmata constitute a network which is able to transmit APs in different directions. Plasmodesmata are relays in a signaling network at the local level. Long-distance information transmission in plants is provided by electrical communication via the phloem, phloem parenchyma or protoxylem (Fromm and Bauer 1994, Rhodes et al. 1996, Dziubinska 2003, Lautner et al. 2005). Wide pores in the sieve plates between the sieve-tube elements represent low-resistance corridors for rapid propagation of electrical signals along the plasma membrane of sieve elements (Fromm and Lautner 2006). These features together with a high degree of protection (caused by symplastic isolation) from external interference make the sieve-tubes an ideal candidate for the transfer of electrical signals (Rhodes et al. 1996). Thus, vascular bundles seem to fulfil similar function as nerves, i.e. they enable the propagation of an excitation (action potential) from cell to cell. Electrical signals can leave the phloem pathway at any site via plasmodesmata to induce particular physiological responses in the neighbouring tissue. Even though plant and animal APs share many similar features, there are also many differences between them. Compared to animal APs, plant APs are much slower, lasting for seconds rather than milliseconds. If the plant cell is excited, the AP usually propagates at a rate that is about thousand times lower than the rate of AP propagation along the squid axon. For example in Vitis vinifera, the transmission speed of AP was reported to be about 10 cm s-1 (Mancuso 1999). The refractory periods were found to be much longer in plants than in animals, in the range between 10 min and 5 h (Zawadski et al. 1991). In addition, the initial depolarization of the membrane before AP generation in plants is due to an efflux of Cl- ions rather than an influx of Na+ ions observed in animals (Thain and Wildon 1992). In the animal nervous system, AP sends information from one location to another without affecting the intervening tissue – like a telephone system. By contrast, both the AP and variation potential (VP) in a plant quickly inform as much plant tissues as possible so that all the intervening tissue is informed – like a megaphone message warning everyone within hearing distance (Davies 2004). 2.2.2. Variation Potential 2.2.2.1. Generation and Propagation of Variation Potential Variation potentials (also called slow wave potentials, Stahlberg and Cosgrove 1996) are characterized by kinetic appearance different from that of APs. Although both APs and VPs are called “electrical signals” and both are connected with membrane potential changes, a huge difference exists between their origin and characteristics. On the contrary to AP, VP is

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not a long-distance, self-propagating electrical signal. Instead, it appears to be a local consequence of a systemic signal (hydraulic or chemical), which is transmitted rapidly in the vascular bundles and which elicits local electrical changes along its pathway (Davies 2004). The origin of VP is still ambiguous and chemical and/or physical signals can be possibly involved in its generation. Many studies have suggested that chemical messengers are released from the wounded region and travel throughout the plant, possibly via hydraulic dispersal. The feasibility of this hypothesis has been confirmed by experiments showing that chemical substances applied to the petioles of excised leaves are rapidly (within minutes) transported through the plant (ABscisic Acid - ABA, sucrose, Malone et al. 1994b, Rhodamine B, Hlaváčková et al. unpublished results). When these messengers reach living cells in remote leaves, they activate ligand-modulated ion channels/pumps and the subsequent ion fluxes through plasmatic membrane cause local electrical activity known as VP (Pickard 1973, Van Sambeek and Pickard 1976b, Malone 1996). The nature of these chemical compounds (electrogenic substances) is not known yet although some attempts at their identifications have already been made (Stahlberg and Cosgrove 1996, 1997a). The first experimental results supporting the hypothesis of the existence of primary chemical signal were done by Ricca (1916). He cut a Mimosa stem and reconnected the two cut pieces with a water-filled tube. Flamestimulation of leaf located on lower part of the stem caused an excitation response in the upper shoot. Thus, he proposed that an agent (called as Ricca´s factor, Van Sambeek and Pickard 1976b) inducing leaf folding was able to pass through the tube. Houwink (1935) provided strong evidence that the passage of Ricca´s agent in the xylem of Mimosa produces in adjacent tissue an electrical response described as variation potential. However, it has to be kept in mind that a possible moving agent in Ricca´s experiment did not necessarily need to be of a chemical origin. As has been discussed (see Chapter 2.1), hydraulic pressure surge is transmitted rapidly in the xylem after local wounding and this physical signal can also initiate VP. Pressure changes in xylem sensed by surrounding living cells can trigger changes in the activity of their mechano-sensitive channels or pumps. The resulting altered ion fluxes across the plasma membrane are then monitored as a change in apoplastic potential, VP (Stanković et al. 1997). This hypothesis is supported by results of Malone and Stanković (1991), who demonstrated that, in the absence of wounding, pressure waves imposed at the tip of one wheat leaf can travel to neighbouring leaves, where they are able to induce changes in apoplastic electrical potential similar to VP. Similar results were reported for pea epicotyls after application of xylem pressure to the root of intact pea seedlings (Stahlberg and Cosgrove 1997a) and for distant tomato leaves after externally applied air pressure (Stanković and Davies 1998). In addition, the increase in thickness of wheat leaves (reflecting wound-induced hydraulic signals) (Malone 1992) and a petiole elongation followed by a massive, long-lasting petiole contraction of tomato (Stanković and Davies 1998) shown in tissue distant from the wound site preceded the changes in surface electrical potential (VP). The tissue deformations apparently resulted from a pressure surge rapidly transmitted through the xylem. Actually, the cooperation of physical (a pressure surge) and chemical (messengers) signal may be required for the initiation of VP. Transport of chemical substances by hydraulic surge (“hydraulic dispersal”, see Chapter 2.1) evoking pressure changes in surrounding living cells is supported by the fact that chemical substances can spread throughout the plant very quickly and also in basipetall direction (Malone et al. 1994b, Hlaváčková et al., unpublished results

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with Rhodamine B), which seems to exclude common phloem or xylem transport. Moreover, previous work (Malone et al. 1994a) showed that neither the mass flow itself, nor the associated pressure changes itself induce the systemic response (the proteinase inhibitor activity). Thus, it is conceivable that the hydraulic transmitted mass flow induces local pressure changes and also distributes rapidly and systemically a chemical messenger from the damaged cells throughout the plant, both together resulting in VP.

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2.2.2.2. Main Characteristics of Variation Potential and its Comparison with Action Potential in Plants VPs are not ubiquitous, but characteristic signals for higher plants that are missing in lower plants and animals. VPs have been reported in a variety of plant species in response to strong, damaging stimuli such as wounding (e.g. heat treatment or crushing, Van Sambeek and Pickard 1976b, Malone and Stanković 1991, Stanković and Davies 1998) or to localized increase in xylem pressure (Malone and Stanković 1991, Stahlberg and Cosgrove 1997a). Many characteristics of VP suggest its hydraulic origin and enable to distinguish between AP and VP. In contrary to AP: 1) VPs are associated with the systemic changes of the diameter and length of shoots (Stanković et al. 1997, Mancuso 1999). 2) VPs are not stopped at dead regions of tissue, they are transmitted in the xylem (Davies et al. 1991, Mancuso 1999). 3) When xylem tension becomes negligible (as in plants kept at saturating humidity), VPs are not generated (Mancuso 1999). 4) The amplitude and propagation velocities of VPs decrease with increasing distance from the wounded site (Davies et al. 1997, Mancuso 1999), which is in agreement with decreasing amplitude of hydraulic pressure surge. Thus, unlike APs, VPs do not follow an all-or-nothing rule. 5) The shape and duration of VPs are completely different from those of APs (cf. Figure 2 A, B, Davies et al. 1991, Davies et al. 1997, Stanković et al. 1998). The VPs show wave-like rather than pointed signal shape. This is caused by slower membrane repolarization during generation of VP, which is the reason why VPs are also called “slow wave potentials” (Stahlberg and Cosgrove 1996). A turgor inhibited H+ pump (see point 6) could explain the slower repolarization of VP. 6) The generation of VPs is mainly attributed to a transient shutdown of the H+ pump located in the plasma membrane (Stahlberg and Cosgrove 1996, Stahlberg et al. 2006), whereas the initiation of APs has been shown to involve mainly the opening of ion channels (Stahlberg and Cosgrove 1997a, Stahlberg et al. 2006). This may also explain why the repolarization of the membrane during VP is much slower than during AP (see point 5). 7) VPs share with APs a refractory period. Repeated pressure applications to pea root caused a transient (s-min) increase in epicotyl growth rate but only the first pressure application generated a VP. Even after hours, it was not possible to induce another VP (“slow wave potential”, Stahlberg and Cosgrove 1996). Sometimes several spikes, putative APs, can be superimposed on VP signals (Figure 2, Figure 4b) (Roblin 1985, Stahlberg and Cosgrove 1997b, Stanković et al. 1998). This finding Devane, Robert T.. New Plant Physiology Research, Nova Science Publishers, Incorporated, 2009. ProQuest Ebook Central,

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suggests a possibility of an interaction between VPs and APs. However, the exact conditions leading to AP generation have not been determined, since the appearance of APs is extremely variable. Since the membrane depolarization during VP lasts longer than during AP, VP may be more effective in triggering the opening of excitable channels needed for AP induction. In contrary, depolarization has never been reported to cause a VP suggesting that APs are unable to trigger VPs (Stahlberg et al. 2006).

Figure 2. Action potentials and variation potentials evoked in Helianthus annuus. At the time point indicated with the vertical line, (A) the plant was stimulated electrically at the base (2V, 2s) inducing AP in the above stem or (B) the tip of an upper leaf was stimulated by heat wounding for about 2s inducing VP in the below stem. The resulting VP is accompanied by spikes of AP. For illustrative purposes modified from Stanković et al. (1998), with permission.

2.2.3. Methods of Electrical Signals Measurements A propagation of electrical signal through a plant can be measured by multiple electrodes attached to different sites of a plant body (“plant electrocardiography - ECG”). Electrical signals can be detected by monitoring of changes in either extracellular (EEP) or intracellular electrical (IEP) potential. While EEP reflects apoplastic ion concentration, the IEP reflects the membrane potential changes of an individual cell. Brief overview of methods of electrical signal measurements can also be found in Davies (2006) and Fromm and Lautner (2007). 2.2.3.1. Extracellular Electrical Potential Measurement Extracellular electrical potential (EEP) changes can be measured either non-invasively, by attaching an electrode to a plant surface, or invasively, by piercing a thin electrode into a plant tissue. Invasive and non-invasive methods often give similar results (Mancuso 1999), however, it is necessary to keep in mind the advantages and disadvantages of both methods when choosing one of them for electrical recordings. Surface contact electrodes are non-invasive for plant tissue, which is important for studying of wound responses. They have been commonly used for electrophysiological measurements for several decades (Van Sambeek and Pickard 1976b, Malone and Stanković

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1991, Mancuso 1999, Hlaváčková et al. 2006, Ilík et al. 2009, submitted results). After connection of the surface electrodes to a plant, the contact has to stabilize for some time, typically for one or two hours. The electrode-plant contact is stable only for several hours, which is one of the disadvantages of surface electrodes. Methods for measurements of the surface electrical potentials and types of surface contact electrodes are summarized in our currently submitted paper (Ilík et al. 2009, submitted results). According to our experimental observations, the chosen type of conductive gel/solution plays very important role during the measurement of EEP using Ag/AgCl surface electrodes. When we connected surface electrode with the leaf blade by the drop of 0.3 M KCl, the leaf tissue became slightly damaged within a few hours. In addition, the drop of KCl dried out quite soon and sometimes even ran out from the area of the electrode-leaf contact. Therefore, during the two hours long experiment it was necessary to continuously add the KCl solution in order to keep the contact functional. This problematic dessication of electrode-plant contact can be avoided using bath electrode. In this case, an Ag/AgCl-pelleted electrode impaled into an agar block with KCl is immersed into a saline bath surrounding a plant surface (e.g. leaf petioles) (Rhodes et al. 1996). Another solution of this problem was proposed by Mancuso (1999), who simply connected the Ag/AgCl-pelleted electrode to the plant surface by a conductive gel commonly used in electrocardiography (ECG). With this gel no damaging changes on leaf blade were visible after several hours of measurements and even a small amount of conductive gel was sufficient to maintain the contact for many hours without any further treatment (Hlaváčková et al. 2006). The invasive method of EEP measurement has a big advantage over the non-invasive method, because it ensures a contact between the electrode and the plant tissue that is stable for as long as several days. On the other hand, piercing of thin electrode damages plant tissue and therefore it is necessary to leave the plant enough time to recover from the injury. Generally, the electrode-plant contact requires longer stabilization than in the case of a noninvasive EEP measurement. Many researchers (Zawadski et al. 1995, Stanković et al. 1997, Mancuso 1999, Dziubinska et al. 2001) have already used piercing of thin electrodes into a plant tissue for electrical recordings.

2.2.3.2. Intracellular Electrical Potential Measurement Intracellular electrical potential (IEP) is commonly measured using microelectrodes (Filek and Kościelniak 1997, Herde et al. 1998b, Koziolek et al. 2004, Kaiser and Grams 2006). On the contrary to surface potential measurements, the using of microelectrodes is more technically and skill demanding, as the microelectrode must be inserted (using a micromanipulator) into the cytoplasm of an individual cell. It has to be kept in mind that the insertion of microelectrodes into plant cells can result in artefacts, such as underestimation of the electrical membrane potential due to leaky seals. However, these artefacts can be largely avoided by employment of microelectrodes with a very small tip (150nm, glass capillaries) (Herde et al. 1998b). Even though this method of IEP measurement is precise, it cannot be used universally and its application is mostly limited to large plant cells. A method using severed aphid stylets has been recently developed for phloem IEP recordings (Lautner et al. 2005, Fromm 2006). First, aphids are allowed to settle on a plant and penetrate the phloem sieve tube. After that the aphids are severed from their stylets (by shots from a laser beam) and a glass microelectrode with tip diameter lower than 1μm can be inserted (by using the micromanipulator) into the aphid´s mouthparts, which enables direct

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connection of the microelectrode to the sieve tube. This method enables direct measurement of membrane potential in phloem sieve tube cells in plants and trees attacked by aphids.

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2.2.3.3. Technical Aspects of Electrical Signals Measurements The measurement of both EEP and IEP require the presence of a reference electrode to create a complete circuit (Figure 3). Basically, there are two possibilities where the reference electrode can be placed. When it is attached to a certain part (different from the measured one) of a measured plant, then the detected potential changes are relative. However, when the reference electrode is impaled in wet soil or other root medium and grounded, it is possible to detect absolute changes.

Figure 3. Left side: scheme of experimental set-up of electrical signal (transmitting through the whole plant) measurement by using multiple measuring electrodes attached on untreated leaves and reference electrode placed in the root medium of tobacco plants. Measurement was performed in Faraday cage. Right side: Electrical recordings of the extracellular electrical potential (EEP) changes between electrodes placed on the untreated leaves (E1- the 5th leaf, E2- the 4th leaf, E3- the 3rd leaf, E4- the 2nd leaf) growing below the treated one and the reference electrode placed in the root medium. The EEP changes were detected during an hour after local burning (time = 0 min, arrow) of the upper (6th) leaf of tobacco plants.

Since the maximum measured amplitudes of plant electrical signals do not exceed several tens of milivolts, the measuring devices must have high input resistance (1012 - 1015 Ω) and their resolution should be at least several tens of microvolts. To detect a complex electrical signal spreading throughout the whole plant, the signal from multiple electrodes placed in different parts of a plant body must be collected simultaneously (Figure 3). The output signal

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from the voltmeter is transferred to an analog/digital PC data converter (data acquisition card inside a computer). The electrical recordings are stored and handled by a computer software. Recently, an electrophysiological workstation that is able to register electrical activity in real time with 0.01 ms resolution has been developed (Volkov 2006). Detection of weak bioelectric signals is sensitive to changes in external electromagnetic field. Any swinging mains or plugged electrical device around a plant can induce electrical potential changes on a plant and affect the measurement of electrical potentials. This can be avoided by placing the studied plant (and in some cases also the measuring device) inside a Faraday cage (Figure 3) which is grounded together with the reference electrode.

2.3. Physiological Roles of Physical Signals in Systemic Wound Responses

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The demonstration that the wounding of a plant evokes the generation of physical signal that propagates to the areas distant from the wounded one would be of a little interest if this signal did not lead to systemic physiological plant responses. Physiological significance of electrical signals in plants has also been reviewed by Fromm and Lautner (2007). Here, I will focus my attention on a detailed analysis of the role of physical signals in the induction of leaf movement, gene expression and protein synthesis, photosynthesis and respiration.

2.3.1. Leaf Movement Leaf movements of carnivorous and mechanosensitive plants are among the bestdocumented consequences of long-distance electrical signal propagation in plants. For example, some carnivorous plants use electrical signals to induce rapid leaf or tentacles movement for capturing insects in order to supply nitrogen. Electrical signaling actions in carnivorous or mechanosensitive plants have been extensively reviewed and investigated elsewhere (Sibaoka 1969, Pickard 1973, Thain and Wildon 1992, Trebacz et al. 2006, Volkov et al. 2008) therefore I will present here only a brief overview of the mechanism of electrical signals generation and action in these plants. One of the best known carnivorous plants is Dionaea muscipula, whose leaves consist of two lobes and in the centre of each lobe there are three multicellular trigger hairs. Pushing of any of these hairs by insect leads to the generation of AP, which spreads over the leaf with a velocity of approximately 100 mm s-1. If two propagating APs are initiated in this way within a short period of time (less than 40s), the two lobes of the leaf close together rapidly and trap the insect. Such double-excitation-triggered trap closure protects the plant against accidental stimulation and ensures that the trap only closes around a living prey. A very similar insect trapping mechanism can be found also in the aquatic plant Aldrovanda vesiculosa, however, it shuts down its traps after a single stimulation of a hair. The leaves of Drosera plants carry many multicellular tentacles, each of which has a globular head that produces a sticky fluid containing digestive enzymes. Mechanical stimulation of tentacles by insect causes the generation of AP in the cells of the sensitive tip. When the AP, propagating at a rate of about 5 mm s-1, reaches the base of the tentacle, the tentacle wraps itself around the insect. At the same time, the action potential propagating to neighbouring tentacles and further movement of the insect on the leaf surface stimulate other tentacles to bend over and trap the insect with their sticky mucilage (fluid).

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Leaves of mechanosensitive plant Mimosa pudica consist of several paired leaflets (pinnae), each of which is divided into paired minor leaflets (pinnules). There is a motor organ (pulvinus) at the base of each pinulle and pinna and also at the junction of the petiole with the stem. Stimulation of the pinnules initiates AP that travels to the pulvinus, where it evokes ion and water fluxes between extensor and flexor cells. As a result, the pinnules close together in pairs. If the stimulation is strong enough, the petiole bends downwards making the leaf look like dead and thus unappealing to herbivores.

2.3.2. Protein Synthesis and Gene Expression It has been shown many times that electrical signals generated in response to local wounding play important role in the systemic induction of protein synthesis and gene expression. Among the best studied defensive proteins that are synthesized in response to either herbivore, pathogen attack or even abiotic stresses are proteinase inhibitors proteins. The first unequivocal evidence of a link between an electrical signal and a biochemical response in plants was given by Wildon et al. (1992), who showed that electrical signals are directly involved in turning on proteinase inhibitor (pin) genes in tomato. The inhibition of phloem flux of tomato seedlings affected neither the systemic accumulation of pin transcripts and pin activity, nor electrical signal propagation. Thus, they excluded movement of chemicals out of the wounded tissue. Moreover, the observed electrical signal was originally described as AP (Wildon et al. 1992), however, later Davies (2004) and even Wildon himself and his co-workers (Rhodes et al. 2006) corrected this misunderstanding and concluded that flame wounding of tomato invariably evokes variation potential of hydraulic origin. Therefore, electrical events and even accumulation of pin transcripts could be responses to chemicals transported in the xylem by hydraulic dispersal from the wounded site. Nevertheless, despite the misunderstandings concerning the different types of electrical signals in tomato plants, the report of Wildon et al. (1992) helped to make the study of electrical signals more respectable and closer to mainstream biology (Davies 2004). Davies et al. (1997) showed that a heat wounding of tomato plants is able to evoke VP, whereas electrical stimulation occasionally evokes APs. Both of these signals were shown to induce accumulation of mRNA encoding proteinase inhibitors (pin1 and pin2). It has been found that in leaves that received either AP or VP, the levels of pin2 mRNA were 4- to 6times higher than in the control plant. Interestingly, leaves from treated plant which did not receive any AP did not show any pin2 mRNA accumulation. Furthermore, since an increase in mRNA can be seen within 5 min and in one case is maximal at 5 min in tissue about 5 cm from the region stimulated, the signal travelled at a rate exceeding 10mm min-1. The authors have concluded that such fast signal propagation would be unlikely if the initial signal is a hormone transported in the phloem and xylem. Therefore, they suggested that the VP is generated as a response to heat-induced hydraulic surge. Stanković and Davies (1996) also reported that hydraulically (flame-wounding) induced VPs and electrically induced APs are capable of evoking pin2 gene expression in tomato plants. Whenever there was no electrical signal (or only a very small signal of less than 8mV) detected in the petiole of the analyzed leaf, pin2 mRNA level remained low. Herde et al. (1998a) provided time-resolved analysis of signals involved in systemic induction of rapid (30 s to 30 min) pin2 gene expression after heat treatment, electrical stimulation and mechanical wounding of a plant. They concluded that the action potential is sufficient to slightly induce pin2 gene expression and the variation potential or the decrease in turgor

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pressure seemed to induce a significant stimulation of pin2 gene expression in tomato plants. Moreover, the results of Herde et al. (1995) clearly show that direct current application to tomato leaves initiates pin2 mRNA accumulation detected locally and systemically in 5 h after stimulation. The capability of AP to affect gene expression is supported also by recent study of Felle and Zimmermann (2007), who demonstrated that long-distance propagated APs in barley plants, generated as a response to the application of mild salt stress or amino acids, were accompanied by a transient increase in apoplastic pH and decrease in cytoplasmic pH. The apoplastic alkalinization is interpreted by the authors as an indicator of stress (Felle et al. 2005), whereas the cytoplasmic acidification may serve as a precondition for upregulating genes or could act as a trigger for gene activation (He et al. 1998). Except of the induction of pin genes, also the expression of calmodulin genes seems to be inducible by electrical signals. After burning the hypocotyl of Bidens pilosa, calmodulin mRNA accumulation takes place in distant, unwounded tissue (Vian et al. 1996). Distant tissue, which showed no change in membrane potential, showed no change in calmodulin mRNA accumulation. In contrast, when a change in membrane potential was evoked in distant undamaged tissue by local burning, an accumulation in calmodulin mRNA occurred 20 min later. Authors proposed that VP evoked calmodulin mRNA accumulation at a distant unwounded tissue. Davies et al. (1997) supported this hypothesis by showing of the VP propagation followed by the rapid (within minutes) increase in calmodulin mRNA accumulation in distant undamaged tomato leaves after local burning. The accumulation of calmodulin mRNA following the VP may indicate that cytosolic Ca2+ is increased in response to an injurious stimulation. Heat wounding (burning by lit match) of tomato also evoked a systemic decrease in polysomes (i.e. polyribosomes, a cluster of ribosomes, bound to a mRNA molecule) and their protein synthesizing capacity in vitro. Very little of the newly-synthesized pin and calmodulin mRNA was recruited into polysomes during the first hour following wounding (Stanković and Davies 1998). According to authors, since the appearance of VP in distant tissue preceded the systemic molecular responses, the VP might be the long-distance signal up-regulating transcription of pin and calmodulin, and down-regulating translation. In addition, Davies (2004) have identified a putative local signal (second messenger- inositol phosphate) that could have been evoked by the systemic VP, and which could, in turn, evoke rapid (seconds and minutes) transcript (encoding the - ribulose-1,5-bisphosphate carboxylase/oxygenase Rubisco small subunit) accumulation. It is important to point out that in some cases electrical signals did not seem to be sufficient in triggering pin2 gene expression upon different stimuli. Data of Herde et al. (1996, 1999a) obtained with ABA-deficient tomato mutants strongly suggest that a minimum threshold concentration of ABA within the plant is required for the early events in electrical signaling and mediation of pin2 gene expression upon wounding and electrical stimulation. An important role of ABA in the electrical signal generation and propagation confirmed also our results obtained with locally burned wild-type (WT) and ABA-deficient tomato mutants (Hlaváčková et al. 2009, submitted results). Heat-induced pin2 gene expression and membrane potential changes seemed to be dependent on the accumulation of jasmonic acid (JA, Herde et al. 1996, 1999a).

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2.3.3. Photosynthesis,stomata and chloroplast movement A few studies published several decades ago showed that the local burning of various plants may generate electrical signals propagating through the plant, triggering the decrease in the gas exchange parameters in distant leaves (Gunar and Sinyukhin 1963, Van Sambeek and Pickard 1976a). Thereafter, the investigation of the relation between photosynthesis and electrical signals extinguished for several decades. In 1993, Fromm and Eschrich detected electrical signals followed by shifts in CO2, O2, H2O exchange and in chlorophyll fluorescence parameter FV/FM (potential maximal quantum efficiency of photosystem II photochemistry, designated by the authors as Fv/Fmax) in willow leaves after root stimulation. Different stimuli (application of auxins, cytokinins, ABA, acidification) evoked different electrical signal (with respect to its shape, amplitude and direction) propagated from the root to the leaves corresponding with different systemic leaf response. Their experiments clearly showed that the non-electric (photosynthetic) responses depended on the shape, amplitude and sign (positive or negative) of the electrical signal (response). Shortly thereafter, studies of the gas exchange relaxation kinetics in tomato plants (Herde et al. 1995, Peña-Cortés et al. 1995) support and extend previous reports about the participation of electrical signal in long-distance information transfer leading to photosynthetic response. Authors showed that both mechanical and electrical excitation resulted in fast (within 2-3 min) decreases in the assimilation and transpiration rates. A mild delay (a few minutes) of the responses was observed in the systemic tissues. According to the authors, the fast electrical signal propagation could refer to the fast (2-3 min) photosynthetic responses. Moreover, rapid (within minutes) changes of chlorophyll fluorescence (photochemical and non-photochemical quenching parameters) and pigment composition detected locally and systemically in tomato plants upon mechanical wounding, electrical current and heat (Herde et al. 1999b) suggest the fast transmitting signal to be of electrical (or hydraulic) origin. After soil drying the maize plants were watered and increases in foliar CO2 and H2O exchange have been demonstrated to follow the arrival of an electrical signal in the leaves from the roots (Fromm and Fei 1998). Observation of dye solution uptake and movement from the root to the leaves after soil irrigation showed that the increase of gas exchange 12-15 min after irrigation could not be triggered by water ascent. The fact that electrical current application evoked changes in systemic chlorophyll fluorescence and pigment composition (Herde et al. 1999b) or gas exchange parameters (Herde et al. 1995, Peña-Cortés et al. 1995) strengthened the hypothesis of a crucial role of electrical signals in long-distance signaling pathways leading to systemic photosynthetic response. Recently, this account was extended by a study of the fast (minutes) systemic inhibition of photosynthesis in Mimosa pudica (Koziolek et al. 2004) upon local flame wounding. Authors demonstrated that electrical signals evoked transient decrease in parameters of chlorophyll fluorescence (the effective quantum yield of photochemical energy conversion in photosystem II, ΦPSII, designated by the authors as ΔF/Fm´) measured by two dimensional imaging system and in the CO2 uptake rate and stomatal conductance. Autoradiographic evaluation of the speed of a chemical signal propagation in Mimosa revealed that chemical signal is much too slow to account for the photosynthetic response after heat stimulation. To contribute to understanding of the role of electrical signaling in trees, poplar shoots were stimulated by chilling and flaming (Lautner et al. 2005). Coldblocking of the stem preventing transmission of the electrical signal via the phloem caused the leaf gas exchange to remain unaffected (Lautner et al. 2005). Direct role of electrical signal in fast systemic gas exchange

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and chlorophyll fluorescence (ΦPSII, designated by the authors as ΔF/Fm´) regulation in poplar upon flame wounding was assumed. In addition, Lautner et al. (2005) proved with calciumdeficient trees and K+ channel inhibitor that calcium as well as potassium is involved in the propagation of electrical signal that evokes the specific responses in the photosynthesis of poplar leaves. Effect of electrical signals on gas exchange parameters are supported also by our results, where the first detected responses of the photosynthetic parameters (5-7 min) were slightly preceded by maximal changes in electrical potential (2-5 min) in systemic tobacco leaves after local burning indicating that the electrical and photosynthetic responses to local burning may be causally linked (Hlaváčková et al. 2006). Similar coincidence was observed in the case of WT tomato plants (cf. Figures 4 and 5). Systemic electrical potential changes started in about 2-3 min after local burning with maximal amplitude reaching at about 5 min after local burning (Figure 4) were followed by a rapid initial increase (followed by the decrease) of parameters of stomatal conductance (gs, Figure 5a) and transpiration rate (E, Figure 5b) and by a rapid decrease of the rate of CO2 assimilation (A, Figure 5c).

Figure 4. Changes in the extracellular electrical potential (EEP) measured between electrodes placed on the burned leaf (a - the 5th), untreated (b - the 4th, c - the 3rd, d - the 2nd leaf) leaves growing below the treated one and the reference electrode placed in the root medium during the first hour after local burning (time = 0 min, dashed line) of the upper leaf of WT tomato plants. Putative spikes of AP superimposed on VP signals are obvious in figure part b. One representative sample is shown, n = 3.

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Figure 5. Response of the rate of CO2 assimilation [A (μmol (CO2) m -2. s-1)], transpiration rate [E (mmol (H2O) m-2 s-1)], stomatal conductance [gs (mol (H2O) m-2 s-1)] of tomato plants to local burning (dashed line). The untreated 4th leaf was measured upon burning of the tip of the 5th leaf, one representative sample was shown, n=3. Arrows indicate times when the actinic light (318 μmol photons m-2 s-1) was switched on and off. Dark respiration (R) was measured 5 min before light on and after light off.

Regarding stomata closure, ion channels participating in the process of stomata closure are activated by both increases in cytoplasmic Ca2+ concentrations and membrane depolarisation (Schroeder et al. 2001, Finkelstein and Rock 2002), both processes are involved in electrical potential changes (cf. Figures 1 and 6) suggesting that electrical signal

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generation and stomata closing may be linked. Direct effect of electrical signal on photosynthetic characteristics at intracellular levels suggested also results of Bulychev and Kamzolkina (2006), who found that electrical signals in Chara corallina are transmitted from plasmalemma to the thylakoid membranes and the fluorescence changes are then evoked by the increase in pH gradient at the thylakoid membrane. The mechanism of AP-induced increase in ΔpH is not yet known, however, authors suggested an increase in Ca2+ level in the cytoplasm after AP generation as its possible cause. The increase in cytoplasmic Ca2+ levels should elevated the Ca2+ levels in the chloroplast stroma, which would suppress the Calvin cycle reactions, thereby decreasing ATP consumption in the dark reactions of photosynthesis. This would lead to the inhibition of ATP synthesis, ΔpH raise and to the deceleration of linear electron flow (Bulychev and Kamzolkina 2006). Thus, an essential role of electrical signals in the regulation of systemic plant photosynthetic response upon local wounding at different levels seems to be plausible. In accordance with previous reports (Koziolek et al. 2004, Lautner et al. 2005), more recently, Kaiser and Grams (2006) demonstrated on Mimosa plants that when the electrical signal arrived at the leaf neighbouring to the burned one, net CO2 exchange started to decline rapidly (within 40-60s) and transiently. Approximately 1 min later, ΦPSII (designated by the authors as ΔF/Fm´) also decreased transiently. Moreover, they presented digital images of stomatal apertures giving evidence that the heat-induced signal causes a rapid, hydropassive stomatal opening response as a result of a depolarization of the surrounding epidermal cells followed by their turgor loss. Later, an active stomatal closure was detected. We also observed rapid (within 10 min) stomata opening followed by stomata closing in the 4th leaf of tomato plants after local burning of the 5th leaf (Figure 5a). Similarly, fast and biphasic systemic responses in the rate of transpiration (in most cases reflecting stomata movement) have already been observed in tomato plants in the leaf located above the burned one (Herde et al. 1995, Peña-Cortés et al. 1995). According to the Kaiser and Grams (2006), stomata of Mimosa did not respond directly to the depolarization of the epidermal membrane potential because their closing response was delayed for several minutes. As for the authors the delayed response was caused by the electric isolation of stomata to the adjacent epidermal cells by the lack of plasmodesmata. Therefore, guard cell deflation was most likely not triggered directly by the electrical signal traveling through the leaf tissue, but by some indirect factors. Regarding the origin of traveling stimulus (AP x VP), their measurements did not allow direct conclusions. But the observation, that not only the motor Mimosa cells but much more tissue is involved in indirect response, makes the idea of a mass transport of fluid carrying a chemical signal (Malone 1993) more credible, because it presents an ample source of water which could be drawn into distant transpiring leaves (Kaiser, personal communication). Moreover, our results indicated that electrical signals (probably induced by a propagating hydraulic signal) may trigger rapid systemic chemical (ABA, JA accumulation) defence-related signaling pathways in tobacco plants after local burning (Hlaváčková et al. 2006). Both electrical and chemical signals were probably interactively involved in the induction of short-term (within minutes) systemic stomatal closure and subsequent reductions in the rate of transpiration and CO2 assimilation after local burning events (Hlaváčková et al. 2006). Therefore, the suggested indirect factors (following the electrical signal) involved in triggering of systemic stomata closing in response to local burning of Mimosa (Kaiser and Grams 2006) might be of chemical origin as in our case. Moreover, the rapid wound-induced hydraulic signals and stimulus transmission was demonstrated by Malone (1994c) in Mimosa.

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New insight in the role of physical signals in the reaction of leaf gas exchange parameters to plant stress gave a recent paper of Grams et al. (2007). They suggested an independent action of both hydraulic and electrical signals in the rapid changes of photosynthesis and stomatal aperture upon re-irrigation of intact drought-stressed maize plants. Their results provided evidence that hydraulic signal spreading through the xylem initiated the rapid (60s after re-irrigation) hydropassive decrease in stomatal aperture, while electrical signals spreading through the phloem induced the gradual (within 10 min – 30 min after re-irrigation) recovery of net CO2 uptake and stomatal conductance upon re-irrigation after drought stress. Because the photosynthetic parameters change systemically upon local effect, one would expect that the movement of photosynthetic organelles - chloroplasts, that are closely linked to photosynthetic efficiency - would also be influenced by the same signal as the changes in photosynthetic parameters. This hypothesis is supported by following results. Changes in the activity of membrane-located mechano-sensitive channels (also known to be evoked after local wounding by hydraulic pressure surges spreading in xylem leading to variation potential generation, Mancuso 1999, Stanković et al. 1997) were reported to influence also chloroplast movement (Sato et al. 1999, 2003a). Wada et al. (1993) suggested local changes in membrane properties, including transient modulation of the membrane potential to be the earliest steps in signal transduction leading to the chloroplast movement. In addition, the time course of chloroplast movement in Elodea canadensis coincided with rapid changes (minutes to hours) in the membrane potential with low amplitudes (4 to 7 mV), recorded by microelectrodes impaled into the midrib of the attached wounded leaf (Gamalei et al. 1994). Authors concluded that chloroplast movement was initiated and enhanced by wound reactions transmitted from cell to cell via plasmodesmata (Gamalei et al. 1994). However, except our recent paper (Nauš et al. 2008), no papers deal with relation of long-distance intercellular systemic signals and chloroplast movements in plants. We tested the hypothesis whether the electrical potential changes spreading from the locally burned or irradiated tobacco leaves could affect chloroplast movement systemically. However, we did not detect any rapid (within hours) systemic responses in chloroplast movement to local irradiance or burning indicating that chloroplast movement in tobacco is dependent mainly upon the intensity and spectral composition of light that irradiate the target tissue (Wada et al. 2003) or upon local mechanical stimulation of the target tissue (Sato et al. 1999, 2003a). Thus, in contrast to systemic photosynthetic and stomatal responses, chloroplast movement is probably regulated only locally, independently on systemic signals (Nauš et al. 2008).

2.3.4. Respiration Stimulation of the base of pumpkin stem by heat or by high KCl concentration evoked electrical potential changes propagating along the stem to the leaves and following by an increase in the respiration rate (Gunar and Sinyukhin 1963). Dziubinska et al. (1989) reported the stimulating effect of excitation on the rate of respiration in the liverworth. The action potential produced by either a cut (a damaging stimulus) or an electrical stimulus (a nondamaging stimulus), caused a transient rise in the rate of respiration. If stimulation did not produce excitation, the increase in the rate of respiration did not take place, regardless of the magnitude and type of the stimulus applied. The results presented by Filek and Kościelniak (1997) indicated a close relationship between the transmission of an electric signal from thermally wounded roots and the rapid (within seconds and minutes) enhanced respiration rate of horse bean seedlings shoots. Local cooling or freezing of the stem inhibited the

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stimulation of respiration, which seemed to be a consequence of damping of the amplitude of the electrical wave reaching the leaf. The shape of electrical potential corresponded with the magnitude and amplitude of the systemic response (Filek and Kościelniak 1997) similarly to the results of Fromm and Echrich (1993) obtained on willow. Electrical signaling seemed to have direct impact on the respiration also in the reproductive system of Hibiscus plants (Fromm et al. 1995). Stimulation of the stigma by pollen, heat wounding or cold block (4◦C) evoked different electrical potential changes in the style propagating quickly (1.3-3.5 cm s-1) towards the ovary and causing different response in the ovarian respiration. Self- and cross- pollination caused a transient increase of the ovarian respiration rate in 3-5 min after the stigma stimulation. In contrast, both cold shock and wounding of the stigma caused a decrease in the ovarian respiration. Experiments with labeled auxin lowered the possibility of the action of chemical compounds in such a fast response. Thus, these results further supported the idea that different, stimulus-dependent electrical signals cause specific responses of the plant metabolism.

3. CHEMICAL SIGNALS

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Next to an effect of electrical signals, chemical signals play also an important role in plant stresss signaling. The term ‘chemical signals‘ covers up a broad range of chemical signaling molecules including also volatile molecules. In this part of the chapter I will focus on abscisic (ABA) and jasmonic (JA) acid, chemical signaling compounds intensively studied in plant stress signaling research. In particular, their effect on photosynthesis, stomatal conductance, protein synthesis and gene expression during plant response to stress will be discussed.

3.1. Abscisic Acid The phytohormone abscisic acid (ABA) is an important compound in the control of plant responses to abiotic stress, notably water deficit. However, ABA levels in vegetative tissues can be elevated in response to various environmental stresses, for these reasons ABA is sometimes referred to as a stress hormone. An important ABA feature is its action not only in the stressed part of the plant but also in distant unstressed parts, therefore ABA is a possible candidate of long-distance stress signal in plants. Although lot of work on the involvement of this hormone to abiotic stress response, especially drought stress, has already been done, the receptor of this hormone was not found until recently. In 2006, Razem and his co-workers have shown that ABA receptor is FCA, an RNA binding protein involved in flowering.

3.1.1. ABA Biosynthetic Pathway and its Localization in Plant Organs and Cells Processes involved in abscisic acid (ABA) biosynthesis and their localization in plant cells and organs have already been reviewed (Taylor et al. 2000, Milborrow 2001, Finkelstein and Rock 2002, Nambara and Marion-Poll 2005, Taylor et al. 2005, Marion-Poll and Leung 2006), therefore I only briefly summarize the main steps of ABA biosynthesis pathway and

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emphasize localization of its biosynthetic steps and connection to possible ABA long-distance transport or action in plants. The biosynthesis of abscisic acid (ABA) is tightly connected with the metabolism of carotenoids (carotenoids cleavage). Carotenoids are derived from five-carbon compounds, isopentenyl diphosphate (IPP) and its isomer dimethylallyl diphosphate (DMAPP). These compounds stand at the beginning of the biosynthetic pathway leading to ABA. IPP can be synthesized both in cytosol and in plastids, however, from different precursors. In cytoplasm the synthesis starts from acetyl-CoA and involves the formation of mevalonic acid (MVA), whereas in chloroplasts the starting compound is glyceraldehyde 3-phosphate (GA-3-P) and pyruvate and IPP is synthesized via the methylerythritol phosphate (MEP) pathway. The latter, chloroplastic pathway is often suggested to be the primary source of IPP precursor for ABA biosynthesis (Marion-Poll and Leung 2006). For example, Milborrow and Lee (1998) isolated intact spinach leaf chloroplasts from protoplasts and found that they incorporated pyruvate and isopentenyl diphosphate into ABA in high yield and mevalonate (MVA in cytosol) in very low yield. Further steps of ABA biosynthesis, leading from IPP and DMAPP to direct ABA precursor xanthoxin, seem to occur inside chloroplasts. Carotenoid cleavage in chloroplasts leading to xanthoxin is followed by enzymatic reactions located in the cytosol. As the final steps of ABA biosynthesis take place in cytosol, xanthoxin is presumed to migrate from plastid to cytosol by a currently unknown mechanism (Nambara and Marion-Poll 2005). Cytosolic conversion of xanthoxin to ABA aldehyde is followed by a final oxidation step leading to ABA (Marion-Poll and Leung 2006, Taylor et al. 2005). One of the well known roles of ABA in plants is its involvement in stomatal closure and therefore the localization and regulation of ABA biosynthesis in guard cells is of particular interest. There are two basic hypotheses explaining the presence of ABA in guard cells. The first hypothesis assumes that guard cell chloroplasts contain apparatus necessary for ABA biosynthesis. The idea of direct ABA synthesis in guard cells is supported by the revealing of the location of AAO3 protein (enzyme for the final step in ABA biosynthesis) and mRNA inside the guard cells (Koiwai et al. 2004). Furthemore, Christmann et al. (2005) revealed by the non-invasive reporter system stomata to be the foci of physiologically active ABA during water stress in Arabidopsis. Even though there is some evidence of ABA biosynthesis in guard cells, Parry et al. (1988) have shown that stomata of tomato plants were unable to convert 2-cis-xanthoxin (referred to as xanthoxal) into ABA. In such case, where does the stomatal ABA come from? Guard cells lack plasmodesmata, however, it is possible that ABA is transported to guard cells from the apoplast. ABA has been previously shown to move through the plant quite readily both in the xylem and phloem (Zeevaart 1977, Munns and Sharp 1993), which makes the apoplastic supply a feasible hypothesis. It is not clear which hypothesis is the correct one, but both processes (ABA synthesis in guard cells and apoplastic ABA supply) of ABA accumulation in stomata seem to be plausible. As has already been mentioned, ABA is mobile and it is detected throughout plant development in all tissues. In well-watered plants, ABA-specific gene expression was localized to the root columella, the cells of the quiescent center and vascular tissues of root and shoot of Arabidopsis (Christmann et al. 2005). Vascular bundles might be the site of ABA synthesis in vegetative organs of well-watered plants, since concomitant expression of AAO3 - ABA biosynthetic enzyme gene has been detected in phloem companion cells and xylem parenchyma cells in Arabidopsis (Koiwai et al. 2004). The localization of ABA

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biosynthetic gene expression in the different root tissue of Arabidopsis (Koiwai et al. 2004) indicates that ABA may stimulate or retard root development in response to various signals. The sites of ABA synthesis and its possible translocation were studied mainly under water stress conditions. Two hypotheses, ABA transport from the root to shoot and ABA synthesis in the shoot as a response to other translocated systemic signals, are supported by following experimental data, which indicates that action of both processes may be possible in plants. Wilkinson and Davies (2002) showed ABA to be synthesized in the roots in drying soil and then translocated to the shoot for regulation of transpiration. Christmann et al. (2005) suggested a rapid export of ABA from roots to shoots, such that ABA generated de novo in the root is efficiently depleted. However, Holbrook et al. (2002) demonstrated by grafting experiments with ABAdeficient tomato roots that stomatal closure does not require ABA production by roots in the condition of soil drying. Authors suggested that a chemical signal released from roots leading to a change in apoplastic ABA levels in leaves may be responsible for the stomatal closure. In-vivo imaging of ABA pools indicated an elevation of ABA levels in the shoot rather than in the root exposed to water stress in Arabidopsis, ABA accumulation in the shoots preceded that in roots (Christmann et al. 2005). Ten hours after the application of water stress to the root system, ABA pools were found almost exclusively in the stomata of the cotyledon and vasculature of the shoot of Arabidopsis plants; the primary sites of ABA biosynthesis seemed to coincide with ABA action (Christmann et al. 2005). Moreover, ABA biosynthetic enzyme gene expression in vascular tissue was demonstrated not only in turgid plants (Koiwai et al. 2004) but also under stress conditions, since ABA levels were significantly increased in these tissues by water stress in Arabidopsis (Christmann et al. 2005). Long-distance signal (negligible amounts of ABA, hydraulic signal or pH changes within the xylem sap) translocated from water stressed root to shoot triggering ABA biosynthesis in the shoot was proposed (Christmann et al. 2005). Koiwai et al. (2004) pronounced the hypothesis that osmotic- and salt-stresses are monitored in the vascular tissues, and the rate of ABA biosynthesis in the vascular tissues and amount of ABA loading are regulated in the companion cells and/or xylem parenchyma cells. Then, the exuded ABA is transported to the target tissues or organs via the sieve element and/or xylem vessels.

3.1.2. Physiological Roles of ABA in Systemic Wound Responses 3.1.2.1. Protein Synthesis and Gene Expression Mechanical damage (wounding), heat treatment or electrical stimulation are able to induce a local and systemic pin2 mRNA accumulation (Herde et al. 1995, Peña-Cortés et al. 1995). However, these treatments of tomato plants induce also a local and systemic accumulation of endogenous ABA and JA (Peña-Cortés et al. 1989, Herde et al. 1996, 1999a), which suggests the involvement of these plant hormones in signaling pathways leading to systemic protein synthesis. This is supported by the finding of Peña-Cortés et al. (1989, 1995), who observed similar local and systemic pin2 mRNA accumulation upon exogenous application of ABA and/or JA to potato or tomato plants. At the same time, ABAdeficient potato and/or tomato mutants were unable to accumulate JA or pin1, pin2 mRNA in response to mechanical damage (wounding) or electrical stimulation (Peña-Cortés et al. 1989, 1995, Herde et al. 1996, 1999a), whereas high levels of pin2 gene expression were found in ABA-deficient mutant and wild-type plants upon exogenous application of abscisic acid

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(Peña-Cortés et al. 1989). These results strongly suggest that ABA is an essential factor acting before JA in signaling pathways leading from mechanical wounding and electrical stimulation to local and systemic pin2 accumulation (Herde et al. 1999a). Except of pin2, there are also other genes that are induced by ABA. Four other woundand ABA- induced genes that encode two additional proteinase inhibitors, the proteolytic enzyme leucine aminopeptidase and the biosynthetic enzyme threonine deaminase were isolated from potato plants in locally wounded or systemic unwounded tissues (Hildmann et al. 1992). Potato mutants impaired in ABA synthesis showed very low levels of accumulation of the ABA/wound responsive genes upon wounding indicating a significance of elevated levels of ABA for induction of these genes in response to plant injury (Hildmann et al. 1992). Exogenous application of ABA increased the activity of chymotrypsin inhibitor (= proteinase inhibitor) in barley leaves (Casaretto et al. 2004). JIPs (Jasmonate-Induced Proteins) of barley leaves appearing abundantly upon JA or sorbitol treatment were also shown to be induced by exogenous application of ABA (Lehmann et al. 1995). ABA should not be omitted in possible signaling pathways leading to heat shock proteins accumulation. Kukina et al. (1995) detected ABA-responsive chloroplast polypeptides in pumpkin cotyledons and attributed some of them to chaperons that prevent plastid protein degradation when the incorporation of the proteins into the thylakoid membrane is disturbed. Based on these experimental evidences, ABA seems to be directly involved in the release of both local and systemic wound signals or, alternatively, may even be the signal itself. Results presented by Peña-Cortés et al. (1989, 1995) are compatible with a hypothesis assuming ABA to be the signal released from the wound site that directly mediates the systemic induction of the pin genes in non-wounded distal tissues of potato and tomato plants. However, it is possible that the involved signaling are more complex and that ABA is just one of the messengers involved in the signaling pathway.

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3.1.2.2. Stomata Movement, Photosynthesis and Respiration Stomata Movement The most well-known and studied function of ABA in plants is its effect on stomata movements. ABA is able to change stomatal aperture and thus regulate the transpiration rate. The presence of ABA simultaneously promotes stomata closure and inhibits their opening (Assmann 1993, Schroeder et al. 2001, Finkelstein and Rock 2002). Stomatal closing requires ion efflux from guard cells. Most ions released across the plasma membrane of guard cells need first to be released into the cytosol from guard cell vacuoles. A brief overview of mechanisms underlying stomata closure is presented in Figure 6 (adapted from Schroeder et al. 2001). ABA induces an increase in cytosolic Ca2+ concentration in guard cells (Figure 6A), which in turn changes the activity of numerous channels and pumps in plasma membrane. Namely the cytosolic Ca2+ inhibits plasma membrane proton pumps and inwardrectifying potassium channels (Kin+) and activates plasma membrane anion channels that mediate anion release from guard cells (Figure 6B). Channel-mediated anion efflux from guard cells is followed by membrane depolarization (Figure 6B). This depolarization then closes the K+in channels and opens outward-rectifying K+ (K+out) channels, resulting in K+ efflux from guard cells (Figure 6C). The ensuing long-term efflux of both anions and K+ from guard cells contributes to loss of guard cell turgor and induces stomata closure (Figure 6C).

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Figure 6. A simplified model of stomata guard cells closing. For details see the text.

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Photosynthesis and Respiration However, ABA does not affect the physiological status of a plant just by lowering the transpiration rate due to stomata closure. It has been suggested that ABA can directly affect photosynthetic apparatus. Raschke and Hedrich (1985) applied ABA to detached leaves of several plant species and ABA usually affected photosynthesis in two ways - through stomata closure, causing a reduction in CO2 supply, and through a direct effect on photosynthetic apparatus. Responses of stomata and photosynthetic apparatus were usually synchronous and often proportional to each other. Therefore, the decrease in stomatal conductance was compensated by lower assimilation rate, which resulted in constant intercellular CO2 concentration (Ci). This was later confirmed using detached leaves of both WT and ABAdeficient tomato plants, where externally applied ABA led to a decrease of rate of CO2 assimilation (A) and transpiration rate (E) with a little effect on the Ci (Herde et al. 1997). Rapid (in about 10 min) local and systemic decrease in A and E after local burning, mechanical damage and electrical stimulation of tomato plants were demonstrated in previous papers (Herde et al. 1995, Peña-Cortés et al. 1995). These changes in photosynthetic parameters authors assigned to the joined effect of ABA and JA. Local and systemic accumulation of both hormones in tomato plants after all three stimuli (Herde et al. 1996, 1999a) supports this statement. However, the authors usually measured the local and systemic accumulation of the hormones following a long time period (6 h) after the treatment (Herde et al. 1996, 1999a), whereas the response of photosynthetic parameters were detected immediately. Our results showed a fast systemic accumulation of ABA in locally burned tobacco plants within 15 min after the treatment and our data clearly show a strong negative correlation between the ABA concentration and A or gs within 15 min after local burning (Figure7 b,d, see also Hlaváčková et al. 2006). The lowering of A in the presence of ABA cannot be simply explained by a decrease in stomatal conductance, because we did not observe any significant changes in substomatal CO2 concentration (Ci, Hlaváčková et al. 2006). This suggests that the limited supply of CO2 due to stomatal closure might be somehow balanced by simultaneous ABA-induced decrease in photosynthetic activity, which is in line with the previous findings of Raschke and Hedrich (1985). However, the negligible changes in Ci can alternatively be explained by the activation of some internal CO2 source - most probably an enzyme carbonic anhydrase (CA, Moroney et al. 2001). The activity of this enzyme, which catalyzes the release of CO2 from bicarbonate, has been shown to be increased in ABA-treated barley plants (Popova et al. 1996) and pea seedlings (Lazova et al. 1999). Thus, increased activity of CA seems to be a photosynthetic response to elevated ABA concentration pointing to a role for ABA in the functioning of the enzyme. However, it is possible that, besides the activation of CA, the limitation of CO2 can be overcame by increased respiration leading to the rise of CO2 levels in the intercellular spaces. Stimulation of respiratory processes was observed e.g. after ABA application to barley (Popova et al. 1987) or after local wounding (cutting or electrical stimulation) of liverworth (Dziubinska et al. 1989). Mechanisms of direct ABA action on photosynthetic machinery were extensively studied by experiments with plants after exogenous application of ABA. Bauer et al. (1976) reported that ABA inhibited Hill reaction activity in isolated chloroplasts of Lemna minor (L.) plants, which was ascribed to the influence of ABA on the electron transport in photosystem II (PSII). Another evidence of the direct effect of ABA on photosynthetic machinery comes from gasometric measurements. It has been shown that the presence of ABA (ABA treatment)

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reduces the initial slope of the Ci-photosynthetic curves (representing response of the photosynthetic rate to the intercellular CO2 concentration), the maximal rate of photosynthesis, the maximal carboxylating efficiency of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and increases CO2 compensation points in barley plants (Popova et al. 1996). Similar results found also Raschke and Hedrich (1985) on detached leaves of several plant species. On the basis of measured photosynthetic saturation curves and Ci, ABA caused (1) a decrease in the carboxylation efficiency of Rubisco (reduction of initial slope of the saturation curve), (2) a reduction of RuBP (ribulose-1,5-bisphosphate) regeneration capacity (reduction of the CO2-saturated assimilation rate) and (3) an increase of the CO2 compensation point (Raschke and Hedrich 1985). The ABA-induced decrease in Rubisco carboxylation efficiency may be caused by the stimulation of photorespiratory pathway, as long-term treatment of barley plants with ABA was shown to increase the activity of Rubisco oxygenase and glycolate oxidase and more 14C was incorporated into the products of photorespiratory carbon metabolism (Popova et al. 1987). Seemann and Sharkey (1987) demonstrated that the biochemical basis for the apparent effect of ABA on Rubisco activity was not the result of reduced substrate availability, decarbamylation of the enzyme or inhibitor synthesis. Several speculative hypotheses about the mechanisms of ABA-action on photosynthetic apparatus were pronounced. The application of ABA may affect indirectly the kinetic properties of Rubisco, as suggested by results indicating a rise in the CO2 compensation points (Raschke and Hedrich 1985, Popova et al. 1987). This may even result from direct effect of ABA on Rubisco conformation (Popova et al. 1987). Eventually, the effect of ABA on photosynthetic apparatus could be caused by the inhibition of the synthesis of some chloroplast proteins. Observed inhibition of accumulation of the chloroplastic rRNAs in pumpkin cotyledons after exogenous ABA-application (Kukina et al. 1985) leads to the assumption that there could be an inhibition of the synthesis of a number of chloroplast proteins, certain photosynthetic enzymes included (Popova et al. 1987). Raschke and Hedrich (1985) proposed that the cellular response to ABA could begin with an activation of an uptake mechanism for H+, leading to a reduction of the pH in the cytoplasm. This may result in lower activity of enzymes involved in Calvin cycle and in lower efficiency of energy transduction at the thylakoid membranes (Raschke and Hedrich 1985). The effect of ABA on the activity of K+-stimulated, Mg2+-dependent plasma membrane ATPases known to be important for stomatal response to ABA may also be responsible for the ABA-mediated changes of the photosynthetic capacity of mesophyll cells (Seemann and Sharkey 1987). Rubisco activity could be inhibited by the presence of high levels of anions (competitive inhibitors of carboxylation with respect to RuBP) resulting from the disruption of the balance of ion fluxes and subcellular ion concentrations (e.g. chloroplastic) evoked by ABA (Seemann and Sharkey 1987).

3.2. Jasmonic Acid Jasmonic acid (JA) and its methylester (MeJA) are involved not only in plant growth and development but also in defense responses of plants against biotic and abiotic stresses. In the last decade, many studies indicated JA to be a key signal molecule in wound signal transduction pathways acting in local and systemic manner.

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3.2.1. Location of JA Biosynthesis in Plant Organs and Cells Processes involved in jasmonic acid (JA) biosynthetic pathways and their location in plant cells and organs have already previously been reviewed (Creelman and Mullet 1997, Wasternack et al. 1998, Wasternack and Hause 2002, Wasternack 2006), therefore I will here only briefly summarize JA biosynthesis mainly in relation to JA localization and its possible long-distance transport. JA and its metabolites, such as methyl ester (MeJA) and amino acid conjugates of JA, are commonly named jasmonates. Jasmonates originate from the precursors 12-oxophytodienoic acid (OPDA) and dinor-OPDA (dnOPDA), which are named octadecanoids. These precursors are formed within the lipoxygenase (LOX) pathway, which is initiated by oxygenation of polyunsaturated fatty acids (PUFAs) and leads to many different products called oxylipins (Wasternack 2006). Plant membranes, especially chloroplast membranes, are rich sources of precursors of JA - PUFAs (linoleic acid or α-linolenic acid) esterified in glycerolipids and phospholipids. Increases in JA probably result from the activation of phospholipases that release PUFAs from membranes (Farmer and Ryan 1992). Plant extracts also contain highly active acyl hydroxylases that can release fatty acids from membrane lipids. Stimuli perception takes place in the plasma membrane. It is postulated that signals (such as elicitors) interact with membrane receptor, which is followed by the production of (13S)hydroperoxyoctadecatrienoic acid (13-HPOT), the JA-intermediate. The initial steps of the octadecanoid pathway are located in the plastid. It is also supported by the fact that majority of early JA-biosynthetic enzymes (lipoxygenase, LOX; allene oxide synthase, AOS; allene oxide cyclase, AOC) are localized in the chloroplast. JA biosynthetic reactions are located in stroma of chloroplasts up to cis-(+)-OPDA, the following reactions occur in peroxisomes, where JA biosynthesis is completed. Therefore, transport of OPDA or its CoA ester is required between chloroplasts and peroxisomes. OPR3, enzyme that catalyzes later step of JA biosynthesis is located in the peroxisomes (Wasternack et al. 2006, Wasternack 2006). Creelmann and Mullet (1997) proposed the circadian rhythm of intracellular location of JA. JA accumulates in chloroplasts during the day (light) because of the increase in pH of stroma of the chloroplast. In contrary, at night JA is released into the cytoplasm, where it could inhibit expression of genes involved in photosynthesis (see Chapter 3.2.2.1). Similar to intracellular localization of JA-biosynthesis, also the localization of JA itself in plant tissues is dependent on the presence of JA biosynthetic enzymes. AOC enzyme was found to be present in plastids of companion cells and in the plastid-like structures of sieve elements (Hause et al. 2003). However, AOC mRNA was found only in companion cells, indicating AOC protein traffic via plasmodesmata (Hause et al. 2003). In addition, the enzymes preceding AOC in JA biosynthesis, LOX and AOS occur in both companion cells and sieve elements (Hause et al. 2003, Wasternack et al. 2006). The localization of LOX, AOS and AOC in sieve elements suggests an amplified generation of JA in vascular bundles (Wasternack et al. 2006), which corresponds with the preferential generation of JA and OPDA in the main veins of wounded tomato leaves (Stenzel et al. 2003). Not only tomato, but also vascular tissues of Medicago truncatula stems carry the capacity to form jasmonates and produce jasmonates after mechanostimulation (Tretner et al. 2008). These results indicate the potential role of JA as a mobile long-distance signal transported in the vascular bundles. The hypothesis is supported by showing that direct transport of JA from wounded leaves of Nicotiana sylvestris (Baldwin et al. 1997, Zhang and Baldwin 1997) and tomato (Li et al.

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2002, Stratmann 2003, Schilmiller and Howe 2005) plants appeared to be responsible for the subsequent systemic responses.

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3.2.2. Physiological Roles of JA in Systemic Wound Responses 3.2.2.1. Protein Synthesis and Gene Expression Jasmonates has been proposed to be key regulators of plant responses to pathogens, insects and wounding. They were shown to activate genes encoding proteinase inhibitors (Farmer and Ryan 1990, 1992, Farmer et al. 1992, Herde et al. 1996, 1999a), antifungal proteins (see review Wasternack and Hause 2002), hydroxyproline- and proline-rich cell wall proteins (Creelmann et al. 1992) as well as enzymes involved in flavonoid biosynthesis (for details see reviews Creelmann and Mullet 1997, Wasternack et al. 1998, Wasternack and Hause 2002). JA and MeJA are also potent inducers of soybean vegetative storage protein (VSP) gene expression (Mason and Mullet 1990, Franceschi and Grimes 1991, Creelmann et al. 1992). Local burning of ABA-deficient tomato and/or potato mutants caused local and systemic JA and pin2 accumulation (Herde et al. 1996, 1999a). In almost all cases studied, symptoms induced by jasmonates coincided with the appearance of novel proteins designated Jasmonate-Induced Proteins (JIPs, Reinbothe et al. 1994). Application of JA or MeJA induced a strong accumulation of transcripts of pin2 or other wound inducible genes, both in wild-type and in ABA-deficient potato or tomato plants (Hildmann et al. 1992, Peña-Cortés et al. 1995). Exogenous JA application also increased activity of trypsin inhibitor (= proteinase inhibitor) in treated and untreated leaves of barley (Casaretto et al. 2004). Delessert et al. (2004) reported that a third of the systemically early-induced (at 30 min after wounding) genes in Arabidopsis thaliana plants that are involved in regulatory processes were induced by MeJA. They found a significant correlation between regulation by MeJA and the regulation of genes systemically induced by wounding (Delessert et al. 2004). These results support a crucial role for jasmonates as an intermediate in the signaling pathway leading from wounding to the transcriptional activation of the genes. Moreover, local and systemic induction of Heat shock proteins (Hsps) acting in abiotic stress responses (Wang et al. 2004) was detected within 8 or 24h after local treatment of single leaves of Nicotiana attenuata plants by heat shock or mechanical damage, but also after local exogenous application of MeJA (Hamilton and Coleman 2001). Increased abundances of Hsp70 and a single small Hsp (sHsp) were detected in untreated leaves from MeJA treated tobacco plants after 24h. Therefore, it is possible that MeJA is involved in longdistance signaling pathways leading to the systemic Hsps accumulation (Hamilton and Coleman 2001). Moreover, JA is able to induce some specific proteins similar to those induced by heat shock (Weidhase et al. 1987). In addition, vapor application of MeJA and methylsalicylate induced the accumulation of sHsp transcripts in tomato fruit correlating with their protection against chilling injury (Ding et al. 2001) and plant MeJA induced heat shock response (Hsp72) even in animal glioma cells (Oh et al. 2005). Even though a number of proteins is up-regulated in the presence of jasmonates, it has to be noted that several other plastid- and nuclear-encoded chloroplast proteins involved in photosynthesis are down-regulated by jasmonates (Reinbothe et al. 1993a,b,c). Jasmonates were shown to suppress the translation of preexisting leaf mRNAs including those for nuclear encoded chloroplast proteins such as the small subunit of Rubisco and several light harvesting

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chlorophyll protein complex apoproteins (Reinbothe et al. 1993c). Large subunit of Rubisco was reported to be downregulated by jasmonates in barley leaves (Wasternack and Parhier 1997) and the synthesis and contents of large and small subunit of Rubisco were distinctly reduced in leaves of rice after the JA-treatment (Wen-Hua and Rui-Chi 1998). It has been suggested that amino acids released from the degradation of plastid proteins, such as Rubisco, might be used for rapid JIPs formation (Weidhase et al. 1987). In concert with changes in gene expression taking place in the plastid compartment (Reinbothe et al. 1993b), these alterations cause characteristic senescence symptoms, such as loss of chlorophyll and degradation of Rubisco and other chloroplast constituents leading ultimately to cell death. Localized cell death prevents the spread of bacteria, viruses and fungi beyond the infection site, a defense strategy that closely resembles the hypersensitive response. According to Creelmann and Mullet (1997), the ability of JA to inhibit expression of genes involved in photosynthesis suggests that jasmonate could help to reduce the plant capacity for carbon assimilation under conditions of excess light or carbon. Inhibition of genes encoding the photosynthetic apparatus under these conditions can help to balance energy absorption and utilization. Some of the excess energy can be dissipated also via the xanthophyll cycle or through other energy-quenching mechanisms (Bilger and Björgman 1990, Demmig-Adams and Adams 1992), however, the capacity of these systems is often not sufficient. Then, the excess of excitation energy may lead to photooxidative damage, including lipid peroxidation. However, the lipoxygenase-mediated generation of JA could induce changes in the cell that prevents further photochemical damage, such as decrease in chlorophyll content resulting in lower amount of absorbed energy. The accumulation of anthocyanins that are stimulated by jasmonates in illuminated plants could also provide some protection against excess radiation (Franceschi and Grimes 1991, Kondo et al. 2001). A decay of cytoplasmic polysomes after a long-term (48h) treatment of barley leaves by jasmonates indicates a general suppression of translation initiation (Reinbothe et al. 1997). This effect is likely due to the interaction of the previously identified jasmonate-induced ribosome-inactivating protein JIP60 with ribosomes. Eventually, the cytoplasmic ribosomes and their ribosomal subunits decline drastically (Reinbothe et al. 1993c). In accordance with localization of JA biosynthesis, high levels of jasmonate responsive gene expression were observed in paraveinal mesophyll cells and bundle sheath cells that surround veins and to a lesser extent in epidermal cells of mature soybean leaves (Franceschi et al. 1983). Within the cells, jasmonate-induced proteins were found in vacuoles, peroxisomes, nuclei, cytosol and even in stromal fraction of chloroplasts of barley leaves (Hause et al. 1994).

3.2.2.2. Photosynthesis, Stomata Movement and Respiration As has been discussed above, JA is known to inhibit the synthesis of several photosynthesis-related proteins. However, JA also evokes changes in chlorophyll content, respiration, stomatal conductance and in a number of photosynthetic parameters. Pigment Content In growing seedlings of barley and oat, JA and its stereoisomers caused a senescence-like bleaching characterized by a decrease in the content photosynthetic pigments (chlorophylls and carotenoids, Miersch et al. 1986). Leaves of potato cv. Sante treated with JA showed

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from 50% to 70% lower content of individual pigments (chlorophylls and carotenoids) except of antheraxanthin, for which 5.8-fold increase was observed (Kovač and Ravnikar 1994). A decrease in chlorophyll a and b content was also reported in rice seedlings leaves treated with MeJA (Wen-Hua and Rui-Chi 1998). Analysis of carotenoid composition in MeJA treated tomato fruits showed that lycopene accumulation was almost completely inhibited whereas βcarotene was present in higher amounts (Saniewski and Czapski 1983, Czapski and Saniewski 1985). Jasmonate-induced loss of chlorophyll and carotenoid contents are mostly connected to growth inhibition and senescence of plants. However, jasmonate induced loss of chlorophyll could also contribute to the protection of photosynthetic apparatus against photochemical damage (see Chapter 3.2.2.1).

Stomatal Effects Barley plants treated with JA showed a decrease in A and reduced activity of Rubisco, whereas the rates of both dark respiration (R) and photorespiration were increased similarly to increased values of the CO2 compensation point and the stomatal resistance (Popova et al. 1988). It has been suggested that the effect of JA on these photosynthetic parameters is indirect and is mediated by the stomatal closure. Under these conditions, partial pressure of CO2 and O2 in the chloroplasts will change, resulting in a changed ratio of the carboxylase and oxygenase activities of Rubisco. Indeed, next to the role of ABA, an inhibitory effect of exogenously applied jasmonates on stomatal conductance of tobacco (Suhita et al. 2003), Arabidopsis (Suhita et al. 2004) and tomato plants (Herde et al. 1997) suggest that ABA and jasmonate transduction pathways leading to stomatal closure involve overlapping signaling elements. However, experiments performed with ABA-deficient tomato plants showed that physiological levels of ABA are required for proper JA-mediated stomatal closure (Herde et al. 1997). Thus, JA does not seem to act in stomata closing per se and jasmonates seem to have only limited effect on stomatal conductance. Moreover, only very high (possibly toxic) MeJA concentrations in the transpiration stream were effective in causing stomatal closure in barley (Horton 1991). Effect on Photosynthesis Following results obtained with wounded, JA-treated and mutant plants allow us to hypothesize that JA, apart from its limited effect on stomata closing, affects photosynthesis directly. Rapid (in about 10 min) local and systemic decreases in A and E after local burning, mechanical damage and electrical stimulation of tomato plants were assigned to the possible action of JA together with ABA (Herde et al. 1995, Peña-Cortés et al. 1995). Recently we have found that pronounced short-term systemic increase (within 1 hour) in the level of endogenous JA after local burning of tobacco plants closely correlated with the decrease in A and gs (Hlaváčková et al. 2006, Figure 7a,c) suggested an inhibitory effect of JA on A next to its effect on stomatal closure (Ci remained almost unaffected). Incubation of detached tomato leaves in JA solution led to a slight increase in Ci and a rapid decrease in A in WT and even ABA-deficient mutants (Herde et al. 1997). Therefore, it seems that JA could inhibit A independently of ABA or stomatal closure.

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Figure 7. Correlations between endogenous concentrations of jasmonic acid (JA) and the rate of CO2 assimilation (A, a, r2=0,96), JA and stomatal conductance (gs, c, r2=0,96), abscisic acid (ABA) and A (b, r2=0,98 during first 15 min) and ABA and gs (d, r2=0,76 during first 15 min) of the 5th leaf during the first hour after burning (time zero) of the upper (6th) tobacco leaf. Mean values ± SD, n = 4 - 5. See also Hlaváčková et al. (2006).

The mechanism of JA effect on photosynthetic apparatus is a subject of intensive research. Over 7 days of continuous treatment of barley seedlings with JA, the capacity of carboxylation and electron transport decreased proportionally to the increase of stomatal resistance (Metodiev et al. 1996), which suggests that the ratio stomatal/nonstomatal limitation of photosynthesis by JA remains largely unchanged. The decrease in the initial slopes and levels of saturation of measured photosynthetic curves observed in the presence of relatively high JA concentration suggests that JA can suppress Rubisco carboxylation activity and lower RuBP regeneration capacity (Metodiev et al. 1996). A and the activity of Rubisco in leaves of rice seedlings were decreased by treating with MeJA (Wen-Hua and Rui-Chi 1998). JA is most probably able to affect photosynthesis even at the level of thylakoid membranes. The long-term JA-treatment of barley seedlings caused an alteration in chloroplast ultrastructure. The number of thylakoids per granum as well as the average length of granal and stromal thylakoids were lower in JA-treated plants (Popova and Uzunova 1996). At the same time, JA-treatment of barley seedlings led to marked quantitative and qualitative changes in polypeptide profiles in thylakoid membrane (Maslenkova et al. 1992). This may be connected with the previously discussed jasmonate induced down-regulation of some nuclear- and chloroplast- proteins involved in photosynthesis (Reinbothe et al. 1993b,c

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Wasternack and Parthier 1997, see Chapter 3.2.2.1). JA-induced alteration at the level of supramolecular organization of the barley thylakoid membranes was also deduced from chlorophyll fluorescence measurements (Ivanov and Kicheva 1993). Low temperature (77K) fluorescence emission spectra revealed JA-induced alterations in the organization and/or composition within pigment-protein complexes of photosystem I (PSI), most probably dissociation of the PSI pigment protein complex CPIa into its components (Ivanov and Kicheva 1993). This finding is in line with the previously reported polypeptide profile of thylakoid membranes isolated from JA-treated barley seedlings (Maslenkova et al. 1992). However, low temperature fluorescence spectra also indicated changes in the molecular assembly and/or composition at the level of the LHCa/b – light harvesting chlorophyll protein complex of PSII in chloroplasts isolated from JA-treated barley (Ivanov and Kicheva 1993). Based on their results the authors propose that JA treatment of chloroplasts increased the efficiency of energy transfer between LHCa/b complex and PSII core complex. On the other hand, the slight decrease in maximal quantum efficiency of PSII photochemistry (designated by the authors as Fv/Fm) with increasing JA concentrations indicates that PSII in JA-treated chloroplasts is less efficient in utilizing the absorbed light energy. It may be caused by some JA-induced alterations in the rates of QA (primary quinone acceptor of PSII) reduction/reoxidation (Ivanov and Kicheva 1993). They assumed that higher F0 (initial fluorescence intensity of the dark-adapted sample) values represented the increased quantity of LHCa/b complex within the thylakoid membrane of JA - treated chloroplasts. The higher values of FV (variable fluorescence) in JA treated thylakoid membranes indicated that the photoreduction of QA could not be involved in the JA - induced reduction of the primary photochemistry of PSII (Ivanov and Kicheva 1993). A direct effect of jasmonates on PSII function was also demonstrated by Maslenkova et al. (1990), who observed a negative (inhibiting) effect of JA on the kinetic characteristics of oxygen evolution and oxygen evolving apparatus in thylakoids prepared from barley. More than 400% enhancement of respiration (μl O2/h/g) detected Satler and Thimann (1981) in MeJA-treated oat leaf segments.

4. INTERACTIONS BETWEEN PHYSICAL AND CHEMICAL SIGNALS IN LONG-DISTANCE SIGNALING OF PLANTS UPON LOCAL WOUNDING The findings mentioned above indicate that the signaling pathways that trigger systemic responses of plants to local wounding are very complex and involve physical (electrical, hydraulic) and chemical signals. Even though it is possible that these signals may independently induce specific elements of the wound responses, it is more likely that they act in a coordinated, interactive fashion and can affect each other. The possible interactions between physical signals, simultaneous action of hydraulic and electrical signals in longdistance signaling upon wounding and an effect of hydraulic pressure surge on membrane located mechano-sensitive channels in living cells (surrounding the vascular bundles) leading to electrical signal (VP) generation have already been discussed (see Chapter 2.1 and 2.2.2). Following parts of the chapter will be focused namely on the interactions between physical and chemical signals including ABA, JA and also other chemical compounds taking part in

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long-distance signaling upon local wounding (systemin, hydrogen peroxide, ethylene, oligosaccharides, volatiles).

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4.1. Physical Signals, JA and ABA Several experimental evidences suggest that there is some connection between physical and chemical signals. Possible cooperation of chemical (ABA, JA) and physical signals and their interaction during systemic wound response are discussed in detail in Hlaváčková and Nauš (2007). Accumulation of chemical signals and consequent systemic response in distant leaves might be local response to the passage of fast moving physical signal. Electric stimulation was shown to initiate local and systemic increases in ABA and JA levels in WT tomato plants within 6 hours (Peña-Cortés et al. 1995, Herde et al. 1996, 1999a), indicating that changes in ion fluxes across the plasma membrane can play a role in systemic hormone accumulation. In our experiments we have shown that the rapid propagation of electrical potential changes (VP) in locally burned tobacco plants are followed by fast systemic increase in the endogenous concentration of ABA and JA (Hlaváčková et al. 2006). These results support the previously proposed role of physical signals as the primary signals that precede any biochemical reactions in locally burned tomato (Herde et al. 1999a). It has also been shown that the loss of cell turgor stimulates ABA biosynthesis during the desiccation of plants and stretch-activation of plasma membrane ion channels was suggested as a possible mechanism that couples the cell wall/membrane interactions to transcriptional events (Finkelstein and Rock 2002). This would explain the possible participation of VPs in triggering ABA accumulation, as stretch-activated ion channels and pumps are also believed to participate in the formation of VPs (Stanković et al. 1998; Mancuso 1999). The other type of physical signal that spreads through the plant in a response to local wounding – hydraulic signal – also seems to closely interact with chemical signaling. One possiblity is the translocation of chemical signal by hydraulic dispersal (Malone 1993, Malone 1994c, see Chapters 2.1, 2.2.2.1). Hydraulic dispersal of solutes (Malone 1993) has been reported to transport significant quantities of calcium from the wounded (burning) tomato leaf to other parts of the plant, most probably via xylem vessels (Malone et al. 2002). Calcium is an important ion participating in electrical signal generation (see Chapter 2.2.1.1), thus, its direct role as chemical signal in long-distance signaling (e.g. electrical signal generation) is plausible. Herde et al. (1996) proposed that burning of the leaf might cause a massive hydraulic event, which may influence the stability of the membrane, leading to the ABA-independent accumulation of JA and activation of pin2 gene expression in tomato and potato plants. Various chemical signaling substances are able to interact with physical signaling, namely via their influence on membrane potential changes. For instance, Herde et al. (1999a) showed that electrical stimulation or mechanical wounding can induce changes in the membrane potential of tomato plants only if endogenous ABA concentration exceeds certain threshold value. Exogenously applied ABA was reported to change membrane potential in tomato (Herde et al. 1999a) and to stimulate the propagation of electrical signals from willow roots to leaves (Fromm and Eschrich 1993). The involvement of ABA in the generation and propagation of electrical signals was demonstrated in our experiments with locally burned

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WT and ABA-deficient tomato mutant (sitiens) plants (Hlaváčková et al. 2009, submitted results). We have found that the amplitude of electrical signal in WT plants was two-times higher than in sitiens plants, which seems to be in line with the less pronounced initial membrane depolarization in ABA-deficient tomato compared to WT after heat treatment observed by Herde et al. (1998b). Both results indicate a graduated response in electrical potential changes of tomato plants to different concentration of ABA in intra- and extracellular levels. We have also found that, on the contrary to WT plants, the speed of VP propagation (the highest amplitude) in sitiens plants was dependent on the angle position of measured leaf on the stem with respect to the burned leaf rather than on its distance from the burned leaf (Hlaváčková et al. 2009, submitted results). Thus, ABA seems to influence electrical signal generation as well as mechanisms of its propagation. The generation of VPs is attributed mainly to a transient shutdown of the H+ pump in the plasma membrane (Stahlberg and Cosgrove 1996), which is similar to the inhibition of H+pump by ABA-induced [Ca2+]cyt increases during stomata closing response (Figure 6, Schroeder et al. 2001). This coincidence suggests that one of the mechanisms of ABA action on electrical signal generation can be through the inhibition of H+ pump.

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4.2. JA and ABA Several evidences have been found indicating the possible interaction of ABA and JA. ABA has been shown to influence the metabolism of linolenic acid, the precursor of JA (Abián et al. 1991), and to play a role in the expression of lipoxygenase gene (Melan et al. 1993). These results are consistent with the findings of Peña-Cortés et al. (1995), who demonstrated that JA is located downstream of ABA in the signal transduction cascade leading to pin2 gene expression in wounded potato and tomato plants. We have shown in locally burned tobacco that the endogenous levels of JA in distant untreated leaves started to increase when endogenous levels of ABA peaked (Hlaváčková et al. 2006). Thus, ABA might stimulate the early steps involved in JA biosynthesis and transmit the wound signal to the jasmonate pathway as already proposed Seo et al. (1997).

4.3. Other Chemical Signaling Compounds Except of JA and ABA, a number of other chemical signaling compounds may be involved in the complex long-distance signaling pathways leading to the fast systemic plant response after local wounding. Here, I will give only a brief overview of several of them, which are especially interesting for their presumed interaction with physical signals or ABA and JA. More detailed description can be found in e.g. Bowles (1998), de Bruxelles and Roberts (2001), Rojo et al. (2003), Heil and Ton (2008), Tuteja and Sopory (2008).

4.3.1. Systemin An 18-amino acid polypeptide, named systemin (Pearce et al. 1991), was proposed to be an essential regulatory component of wound induced systemic defense responses in tomato (Ryan and Pearce 1998) and tobacco (tobacco systemin I and II, Pearce et al. 2001, Ryan et

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al. 2002). However, the hypothesis that systemin itself undergoes long-distance phloem transport throughout the plant remains controversial, although its fast (minutes to hours) systemic translocation throughout the plant was documented after application of [C-14] systemin to surface wounds on tomato leaves (Narvaéz-Vasquéz et al. 1995). Recent results obtained from grafting experiments on tomato indicate that systemin acts at or near the wound site and appears to strengthen the systemic defence by amplifying jasmonate synthesis in damaged leaves (Schilmiller and Howe 2005). These results are in agreement with the proposal that systemin and jasmonates interact through a positive feedback loop to propagate the long-distance signal (Ryan and Moura 2002). Systemin alone was not sufficient to trigger the induction of pin2 gene expression in ABA-deficient plant indicating that ABA play a crucial role in systemin activated wound responses together with JA in solanaceous plants (Peña-Cortés et al. 1995). Systemin appears to stimulate woundinduced increases in pin levels also by increasing the pools of JA in tomato (Farmer and Ryan 1992). Another aspect of systemin action on long-distance transport is its effect on transmembrane ion fluxes, resulting in changes in cell membrane potential. Suspensioncultured cells of Lycopersicon peruvianum were shown to rapidly (within minutes) respond to subnanomolar concentrations of systemin by alkalinization of the growth medium and by increased efflux of K+ (Felix and Boller 1995). Similar ion fluxes were observed in isolated tissues from the plants of subtribe solaneae upon their exposure to systemin (Lanfermeijer et al. 2008). H+ influx and K+ efflux were rapidly (2-5 min) and transiently increased and resulted in an alkalinization of the unstirred layer surrounding the cells (Lanfermeijer et al. 2008). In addition, systemin was also shown to evoke rapid (lag period of 30 s to 4 min) and transient depolarization of the tomato mesophyll cell membrane and a transient acidification followed by an alkalization of the extracellular pH of tomato mesophyll tissue (Moyen and Johannes 1996). Systemin induced a rapid (1-2 min after application) transient increase of cytoplasmic free Ca2+ concentration in cells from Lycopersicon esculentum mesophyll (Moyen et al. 1998). Elevated apoplastic Ca2+ concentration observed in wounded tomato plants significantly enhanced the biological activity of systemin, as 100 times lower systemin concentration was required to induce maximal proteinase inhibitor accumulation (Dombrowski and Bergey 2007). These data indicate a positive feedback between Ca2+ ions accumulation and systemin action. These results suggest that systemin-induced changes in plasma membrane ion transport play a role in the early phases of systemin signal transduction and might represent initial steps in the signal transduction chain leading to wound response. It is tempting to speculate that the rapid induction of massive ion transport leading to depolarization of the plasma membrane in the presence of systemin may trigger changes in the electrical potential similar to that evoked during transmission of electrical signals after local wounding.

4.3.2. Hydrogen Peroxide Hydrogen peroxide (H2O2) is now being recognized as one of the most important signaling molecules in plants. Compared to other reactive oxygen species, H2O2 is relatively stable and is able to cross biological membranes, which allows H2O2 to play an important role in the regulation of defense response in plants (Orozco-Cárdenas et al. 2001, Bóka et al. 2007). H2O2 can act as a local signal for hypersensitive cell death, but also as a systemic

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diffusible signal for the induction of defensive genes in adjacent cells in response to biotic stress (Alvaréz et al. 1998). H2O2 generated in response to wounding can be detected at wound sites as well as in distal leaf veins within 1h after wounding, even though maximal systemic accumulation of H2O2 was detected within 4-6h (Orozco-Cardenas and Ryan 1999). In both wounded and unwounded (systemic) leaves of tomato plants, H2O2 was detected mainly in the cell walls of vascular parenchyma and in nearby spongy mesophyll cells 4h after wounding (OrozcoCárdenas et al. 2001). Similar deposits were found in cell walls of leaves of transgenic tomato plants overexpressing precursor of systemin, prosystemin. Strong H2O2 accumulation was detected also in the cell walls of spongy mesophyll cells facing intercellular spaces, a few cells away from the vascular traces (Orozco-Cárdenas et al. 2001). The authors have concluded that the components required to produce H2O2 after wounding were induced by systemin (Orozco-Cárdenas et al. 2001). The elevated levels of H2O2 in the prosystemin transgenic tomato plant detected also Orozco-Cardenas and Ryan (1999). They demonstrated that not only exogenously applied systemin, but also oligogalacturonic acid, chitosan, and MeJA activated the production of H2O2 in leaf veins similarly to wounding. Experiments performed on mutant tomato plants (def1, compromised in the octadecanoid defense signaling pathway necessary for JA synthesis) confirmed that the functional octadecanoid pathway is required for H2O2 generation (Orozco-Cardenas and Ryan 1999). Moreover, highly diffusible H2O2 generated in the vascular tissues was suggested as a possible linker between jasmonates (accumulated in the vascular tissues during systemic response) and physiological responses (e.g. activation of defense genes) in mesophyll cells in response to wounding (Orozco-Cárdenas et al. 2001). Possible signaling connection between reactive oxygen intermediates (superoxide, H2O2, hydroxyl radicals) and physical (electrical) signals has been suggested by Dong and Xu (2006). They have detected an immediate (within 30s) oxidative burst in the leaves of tobacco after cutting the stem as well as after flooding the plant’s roots. The transmitting velocity of the systemic signal was too fast (at least 2-3 mm/s) to be of the chemical origin, and therefore the authors propose that some form of electrical signaling may be involved (Dong and Xu 2006). Moreover, the depolarizing effect of H2O2 was found in Lima bean leaves, where accumulation of H2O2 occurred at high levels in cell walls adjacent to intercellular spaces in the spongy mesophyll, after both mechanical and herbivory damage (Maffei et al. 2006). Mechanically wounded Lima bean leaves reacted fast by a strong transmembrane potential (Vm) depolarization to exogenous application of H2O2 (Maffei et al. 2006). Changes in Vm , modulation of ion fluxes at the plasma membrane and the generation of H2O2 have been demonstrated to be amongst the earliest (seconds to minutes, respectively) cellular responses to wounding by insect feeding (Maffei et al. 2007).

4.3.3. Ethylene Another molecule participating in wound signaling is ethylene, whose biosynthesis (Kende 1993) is induced also by wounding. Ethylene was shown to be produced rapidly (within 30 min) and transiently (basal levels reached at 4h after treatment) in tomato plant after leaf injury or application of oligosaccharides (OGAs), systemin or JA through the transpiration stream (O´Donnell et al. 1996). Induction of ethylene by exogenous JA application and ineffectiveness of exogenous JA in the induction of pin gene expression in the presence of ethylene action inhibitors suggest that ethylene is located downstream of JA in

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the wound transduction pathway. Thus, it seems that ethylene potentiates systemin-activated wound signaling through the octadecanoid pathway in tomato (O´Donnell et al. 1996). In contrast to its role in solanaceous plants, in Arabidopsis thaliana ethylene acts as a cross-talk regulator between JA-dependent and JA-independent wound signaling pathways, determining local and systemic wound-induced gene expression (Rojo et al. 1999). At the wounded site, oligosaccharides repressed the JA-dependent signaling pathway through the production and perception of ethylene. However, JA-dependent signalling pathway remained fully operative in systemic tissues. Thus, oligosaccharide-responsive genes and ethylene were accumulated close to the wound site whilst the largest accumulation of transcripts derived from JA-responsive genes was observed in the systemic tissues (reaching their maximal levels in the systemic tissues after 2h) (Rojo et al. 1999). However, some genes (such as JR3), appeared to be regulated by positive interactions of both ethylene and JA signals in Arabidopsis thaliana (Rojo et al. 1998). Thus, the cross-talk between JA and ethylene signaling pathways may have both positive and negative effects on gene expression during wound responses. The interaction among JA and ethylene defense signaling pathways can be antagonistic, cooperative or synergistic, depending on the plant species, the developmental and physiological state of plant (Rojo et al. 2003). Readers that are more interested in modulation of plant defenses by ethylene and its interaction with other signaling molecules (ABA, JA, salicylic acid) are encouraged to study the following papers e.g. Lorenzo et al. (2003), Veselov et al. (2003), Zhao et al. (2004), Adie et al. (2007). The production of ethylene can be evoked also by physical signals spreading rapidly throughout the plant after local wounding. Vicia faba plants, stimulated by scorching of the upper leaf, generated a long-distance transmitting variation potential with or without superimposed action potential (Dziubinska et al. 2003). In stimulated plants, the level of ethylene production measured in lower, non-stimulated (systemic) leaf was significantly higher than that in the control plant and the difference correlated with the amplitude of electrical response. However, exogenous application of ethylene did not cause any considerable changes in VP or AP, indicating that the electrical signal was the primary wounding response. The authors have concluded that the sequence of ion fluxes registered as an electrical response of a plant to the thermal stimulus was a signal evoking an enhancement of ethylene emission (Dziubinska et al. 2003).

4.3.4. Cell Wall Components / Oligosaccharides Cell wall fragments (including oligosaccharides, OGAs) have also been recognized as local or systemic messengers that regulate the expression of PI (proteinase inhibitor) genes in tomato leaves in defence response (Bishop et al. 1981, 1984). The authors suggest that small OGAs act namely as systemic signals, longer cell wall fragments may participate in local responses (Bishop et al. 1984). Interestingly, Doares et al. (1995) demonstrated that the effect of plant derived OGAs on the induction of proteinase inhibitor accumulation in tomato leaves can be severely reduced by inhibitors of the octadecanoid pathway. This indicates that OGAs (here thought to be local signals) may activate the octadecanoid pathway for JA synthesis, which subsequently triggers the wound responsive gene expression (Doares et al. 1995). The stimulative effect of OGAs on JA accumulation is also supported by the finding that exogenous application of OGAs in tomato plants leads to several fold increase in JA content in leaves within 2 h after application (Doares et al. 1995).

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On the other hand, OGAs were found to suppress the JA-dependent signalling pathways in locally damaged tissue in Arabidopsis plants (Rojo et al. 1999). This is thought to be a result of OGAs-stimulated production of ethylene in the locally damaged tissues (Rojo et al. 1999), such as those positive relationship between OGAs signals and ethylene accumulation was already reported in solanaceous plants (O´Donnell et al. 1996). Except of ethylene, OGAs were suggested to promote systemic H2O2 generation in tomato leaves in response to wounding, although even for this effect a functional octadecanoid pathway was necessary (Orozco-Cardenas and Ryan 1999). Polygalacturonases (PGs, enzymes that release OGAs from plant cell walls) and H2O2 were shown to be woundinducible in leaves of several species indicating that systemic wound signals inducing PG activity and H2O2 are widespread in the plant kingdom (Orozco-Cardenas and Ryan 1999). PGs are probably localized in cell walls of the vascular bundles, which is the site where massive H2O2 formation was observed (Orozco-Cárdenas et al. 2001). The production of OGAs by PG is thought to result in the synthesis of H2O2, which then diffuses out of the vascular bundles to mesophyll cells, where it activates the expression of genes (OrozcoCárdenas et al. 2001). Through its positive effect on H2O2 production in guard cells, OGAs also reduce stomatal aperture in tomato or Commelina communis plants (Lee et al. 1999).

4.3.5. Volatile Compounds Traditionally, most studies have focused on chemical or, to a lesser extent, on electrical signals that travel through the plant vascular system after wounding. In some cases, however, rapid wound response is detected even in distal leaves that do not have a direct vascular connection to the attacked leaf. This indicates that also some other type of signal can be involved in systemic defence responses. Currently, there is an increasing number of evidences suggesting that volatile compounds can act as these alternative long-distance signals within the plants as well as between them (e.g. Baldwin et al. 2006, Farmer 2001, Heil and Ton 2008, Howe and Jander 2008, Karban et al. 2006, Kost and Heil 2006). Green-leaf volatiles (GLV, Heil end Ton 2008), ethylene (Ruther and Kleier 2005), MeJA (Farmer and Ryan 1990, Karban et al. 2000) or terpene (Predieri and Rapparini 2007) may be responsible for the airborne signaling upon wounding. Elucidating the mechanisms by which plants perceive volatile signals is a major challenge for future research. MeJA can be converted back into the active form (jasmonic acid), as has been demonstrated by exogenous MeJA application to Achyranthes bidentata plants (Tamogami et al. 2008). Their study demonstrated that exogenous MeJA activated volatile organic compounds (VOCs) emission in receiver plants by converting itself into JA and JA-Ile (jasmonoyl isoleucine) and initiating a signal transduction leading to VOCs emissions and induction of endogenous JA-Ile and JA-Leu (jasmonoyl leucine), which in turn cause further amplification of VOCs emissions. Moreover, 11C-imaging of MeJA in tobacco revealed that it primarily enters the phloem, but then vigorous exchange was observed between phloem and xylem. This exchange is probably enhanced by the volatility of MeJA, which moved readily between non-orthostichous vascular pathways (Thorpe et al. 2007). In case of other VOCs, preliminary experiments demonstrated that exposition to VOCs can lead to changes in membrane potentials in intact lima bean leaves (Maffei, personal communication, in Heil et al. 2008). This suggests that the dissolving of VOCs in the membranes coupled to interactions with membrane proteins may lead to changes in transmembrane potentials and thereby induce gene activity (Heil et al. 2008).

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Additional dimension of volatiles action in plant defence is so-called “priming”, which means metabolic preparation for a more rapid or robust response to subsequent wounding (Howe and Jander 2008). Plants are primed by low concentration of volatiles, which is not sufficient for the initiation of a defence response, however, such plants are able to respond much faster or more strongly to wounding than unprimed plants (Heil and Ton 2008, Ton et al. 2007). Also self-priming by herbivore-induced volatiles has been described in Lima bean plants (Heil and Bueno 2007) and hybrid poplar (Frost et al. 2007). Heil and Ton (2008) suggested that self-priming by airborne signals prepared the systemic tissues for a rapid response, but full activation of costly defence mechanisms is triggered only after confirmation of the injury by the vascular long-distance signal.

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5. CONCLUSION The aim of this chapter was to summarize the present state of knowledge about the longdistance signaling pathways leading to fast systemic responses of plants to local wounding. It is evident that the long-distance signaling pathways in plants are very complex and that signaling compounds involved are tightly interconnected. Thus, it is still a great challenge for researchers to clarify the detailed mechanisms underlying the systemic wound responses of plants. The components of signaling pathways that have been discussed in detail in this chapter are illustrated in Figure 8. Within the first minutes after local wounding, physical signals are dominant in systemic wound responses. Hydraulic surge generated at the site of wounding is transmitted both basipetally and acropetally through the xylem. Pressure changes or chemical compounds transported by hydraulic surge evoke changes in ion fluxes in surrounding living cells, which subsequently leads to local electrical activity (variation potential). Electrical signal can spread rapidly through the plant also in a form of action potential, which is not directly related to hydraulic surge. In systemic tissue, both variation and action potential can then serve as signals triggering defence responses at cellular level (accumulation of chemical compounds, protein synthesis, gene expression, inhibition of photosynthesis, respiration, stomatal closure etc.). Chemical signals are also essential components of the systemic signaling pathways generated after local wounding of a plant. The capability of chemical signals to evoke physical signals and vice versa has already been demonstrated several times, nevertheless, their interactive cooperation has not been clearly explained yet. Many signaling compounds are generated directly at the site of wounding (JA, ABA, systemin, oligosaccharides, H2O2), where they seem to be involved in the generation of the systemic signal. However, some of them (discussed namely for JA, ABA and H2O2) may even act as the long-distance systemic signals themselves. The compounds can be transported either by fast hydraulic dispersal in the xylem, acting at approximately the same timescale as the physical signals, or by phloem flow, initiating slower systemic responses. Emission of volatile chemical compounds by wounded plants has been recently intensively studied as a relatively new aspect of chemical signaling. Volatiles can act through the air, but can be spread also through vascular bundles (as shown e.g. for MeJA) of wounded plant. Similarly to physical and other chemical signals, volatiles can evoke rapid systemic wound response. When acting at lower concentrations,

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volatiles were suggested to be “danger signals” that help the plant to prepare for the coming attack.

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Figure 8. Scheme of putative signaling pathways involved in generation of rapid long-distance systemic responses of plants to local wounding. For details see the text. ABA – ABscisic Acid, GLV- Green Leaf Volatiles, H2O2 – Hydrogen Peroxide, JA – Jasmonic Acid, MeJA – JA-Methylester

ACKNOWLEDGEMENTS The project was supported by grant from the Ministry of Education of the Czech Republic, No. MSM 6198959215. I thank Prof. Jan Nauš for the critical reading of the manuscript and Dr. Iva Šnyrychová for critical reading of the manuscript and for final correction of the text.

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Wasternack, C.; Stenzel, I.; Hause, B.; Hause, G.; Kutter, C.; Maucher, H.; Neumerkel, J.; Feussner, I.; and Miersch, O. The wound response in tomato - Role of jasmonic acid. J Plant Physiol. 2006, 163, 297-306. Weidhase, R.A.; Kramell, H.M.; Lehmann, J.; Liebisch, H.W.; Lerbs, W.; and Parthier, B. Methyljasmonate-induced changes in the polypeptide pattern of senescing barley leaf segments. Plant Sci. 1987, 51, 177-186. Wen-Hua, W.; and Rui-Chi, P. Effect of jasmonic acid methyl ester on the photosynthesis of rice seedlings. Acta Bot Sin. 1998, 40, 256-262. Wildon, D.C.; Thain, J.F.; Minchin, P.E.H.; Gubb, I.R.; Reilly, A.J.; Skipper, Y.D.; Doherty, H.M.; O´Donnell, P.J.; and Bowles, D.J. Electrical signalling and systemic proteinase inhibitor induction in the wounded plant. Nature, 1992, 360, 62-65. Wilkinson, S.; and Davies, W.J. ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ. 2002, 25, 195-210. Zawadzki, T.; Davies, E.; Dziubinska, H.; and Trebacz, K. Characteristics of action potentials in Helianthus annuus. Physiol Plant, 1991, 83, 601-604. Zawadzki, T.; Dziubinska, H.; and Davies, E. Characteristics of action potentials generated spontaneously in Helianthus annuus. Physiol Plant, 1995, 93, 291-297. Zeevaart, J.A.D. Sites of ABA synthesis and metabolism in Ricinus communis L. Plant Physiol. 1977, 59, 788-791. Zhang, Z.-P.; and Baldwin, I.T. Transport of [2-14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris. Planta, 1997, 203, 436-441. Zhao, J.; Zheng, S.H.; Fujita, K.; and Sakai, K. Jasmonate and ethylene signalling and their interaction are integral parts of the elicitor signalling pathway leading to beta-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J Exp Bot. 2004, 55, 1003-1012.

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In: New Plant Physiology Research Editor: Robert T. Devane

ISBN 978-1-60741-102-4 © 2009 Nova Science Publishers, Inc.

Chapter 3

ROOT WATER TRANSPORT UNDER ABIOTIC STRESS CONDITIONS Ricardo Aroca, Juan Manuel Ruiz-Lozano Dpto. Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín (CSIC), 18008, Granada, Spain.

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ABSTRACT Plants in nature are constantly exposed to several environmental fluctuations, ranging from changes in light intensities to changes in soil water content. Alterations of almost all environmental factors may potentially cause a water deficit on plant tissues. Such water deficit is caused by the imbalance between leaf transpiration rate and root water uptake. In contrast with the amount of research done dealing with the regulation of leaf transpiration rate during abiotic stresses, studies about root water uptake under abiotic stresses are less abundant and controversy. There are two different water pathways inside the roots. Under normal conditions, the more important pathway is the apoplastic one. This pathway compromises the water flowing through the cell walls and it is governed by the transpiration rate. The second pathway includes the water flowing through the cells, crossing different cellular membranes and it is called “cell-to-cell” pathway. The “cell-to-cell” pathway is governed by the osmotic gradient between the soil solution and the root xylem sap, and it becomes predominant when the transpiration rate is restricted, for example under abiotic stress conditions. Both pathways are regulated to some extent by proteinaceous channels called aquaporins. Plant aquaporins were discovered fifteen years ago, and here we will summarize the most recent knowledge about their involvement in root water uptake under abiotic stress conditions. In general, under these conditions root water uptake diminishes. However, each kind of stress has its specific effects and we will detail herein how different abiotic stresses (drought, cold, salt or flooding) modify root water uptake. At the same time, we will describe how different stress-related plant hormones such as abscisic acid or methyl jasmonate, or molecular signals, i.e. calcium or hydrogen peroxide, also modify root water uptake. From the present data we highlight the importance of the knowledge of how root water uptake is governed under abiotic stress conditions in order to achieve plants more tolerant to such stresses.

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INTRODUCTION Since plants are sessile organisms, they need to develop several strategies to cope with environmental changes because they can not escape from them. Any environmental factor causing plant growth retardation or a modification in the normal plant physiology is called stress. Plant stresses can be divided in abiotic and biotic stresses; the latter refers to the stresses caused by living organism. Here we will only focus on abiotic stresses, i.e. when changes of the non living part of the environment cause a stress to the plant. For recent advances on plant biotic stresses readers are referred to Asselbergh et al. (2008) and Dreher and Callis (2007). Abiotic stresses cause several alterations on plant physiology, being one of the most common the stomatal closure. Thus, when plants are exposed to environmental stressors such as cold, water limitation, high salts concentrations in the soil or flooding, they tend to close their stomata (Rood et al., 2003; Aroca et al., 2003a; Loreto and Centritto, 2008). This stomatal closure caused by abiotic stresses consequently diminishes the capacity of plants to take CO2 up for photosynthesis. This diminution causes alterations on the leaf primary metabolism and enhances the production of toxic molecules such as reactive oxygen species. For recent reviews on this topic see Loreto and Centritto (2008) and Flexas et al. (2006).

Root Water Transport

Cytoplasm Plasmodesmata

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Transcellular Path Symplastic Path

Xylem Vessels

Suberin

Cell Wall

Vacuole

Transpiration

Apoplastic Path

Root Cells Symplastic Path CellCell-toto-Cell Path Transcellular Path

Adapted from Steudle and Peterson (1998). Figure 1. Scheme of the different paths involved on the radial root water transport. Little arrows indicate exchange of water among different water pathways.

Since root water uptake is mainly governed by leaf transpiration, when stomatal cells close their pore by abiotic stresses, water uptake is simultaneously reduced (Steudle and Peterson, 1998; Aroca et al., 2001). Water goes through roots from external solution to xylem vessels following three different paths (Figure 1). Under non stressful conditions, water goes mainly by the apoplastic path; that is crossing cell wall pores following a hydrostatic gradient caused by transpiration. However, when stomata are closed by a stressful agent, water goes

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mainly by the “cell-to-cell” pathway compromising water circulating by the cytoplasm and plasmodesmata, and water crossing cell vacuoles. Hence, water goes by the “cell-to-cell” pathway thanks to the osmotic gradient between soil nutrient solution and xylem sap. These three paths are intercommunicated and there is an exchange of water among them as the plant environment changes. Since in developed roots suberin may diminished water permeability of apoplastic path, water molecules need to cross plant plasma membrane at least twice in order to reach xylem vessels. However, it is known that under non stressful conditions, apoplastic path has much less resistance to water flow than “cell-to-cell” path (Steudle and Peterson, 1998; Aroca et al., 2001). For more details on the root composite water transport model see Zhao et al. (2004) and Steudle (2000).

Protein sequences are taken from Johanson et al. (2001). Figure 2. Phylogenetic tree including the four aquaporins groups of Arabidopsis thaliana.

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Our understanding of how water molecules cross living membranes have changed in the last fifteen years since the discovery of aquaporins (Preston et al., 1992; Maurel et al., 1993; Kammerloher et al., 1994). Aquaporins are proteinaceous membrane channels that facilitate the transport of water across cell membranes following an osmotic gradient. Plant aquaporins are divided in four groups based on their sequence homology (Figure 2). The four groups are plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), nodulin like intrinsic proteins (NIPs), and small and basic intrinsic proteins (SIPs). Each subgroup is also subdivided, and for example there are PIP1 and PIP2 subgroups, having each subgroup several different proteins. In fact, in Arabidopsis, maize and rice there are around 30 different aquaporins genes (Chaumont et al., 2001; Johanson et al., 2001; Sakurai et al., 2005). At the same time, each aquaporin group differs in their capacity of transporting water and other small and neutral solutes and in their subcellular localization. For recent reviews see Kaldenhoff et al. (2008), Katsuhara et al. (2008), and Maurel et al. (2008). From all the above information, it is known that the water deficit experienced by plants under abiotic stress conditions is caused by the imbalance between water lost by transpiration and by water uptake by roots, being root water uptake less studied comparing to leaf transpiration. Here, we focused on how root water uptake is as important as leaf transpiration in order to keep water status under abiotic stresses. At the same time, we describe how aquaporins regulate root water uptake under abiotic stress conditions and how several hormones and molecular signals regulate root water uptake. We divided the review in different sections, dealing each one with a different abiotic stress (drought, salinity, cold and flooding), or with different signals as hormones, oxygen radicals or calcium.

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DROUGHT STRESS EFFECTS ON ROOT WATER UPTAKE Soils too dry for crop production cover 28% of the dry land surface, so water limitation is one of the most common factors causing loss in crop production (Bray, 2004). When soil starts to become dry, plant roots detect a diminution of the soil water potential and synthesize chemical signals that are transported to the aerial part by the xylem stream in order to induce stomatal closure. Among these chemicals signals the most widely studied is the abscisic acid (ABA) (Hartung et al., 2005; Zhang et al., 2006). However, most recently, Christmann et al. (2007) has found some evidences supporting the idea that ABA is first synthesized in the leaves when plants experience a water deficit episode. While stomatal closure occurs, root water uptake also decreases by means of several factors such as the drop in soil water potential, the lower hydrostatic gradient caused by transpiration, and the diminution of root hydraulic conductivity (L) (Aroca et al., 2006). A decrease of L upon exposure to soil water deficit has been extensively seen (Martre et al., 2001; Siemens and Zwiazek, 2003; Aroca et al., 2006, 2008; Mahdieh et al., 2008), although in some cases a small stimulation has been observed (Lian et al., 2004; Siemens and Zwiazek, 2004). These discrepancies found in the literature are caused by different water deficit intensities, plant cultivation methods, and plant species used. However, it seems that under moderate drought stress or during the initial phases of drought, plants respond increasing L, and when drought is more severe or more prolonged L decreased (Table 1), although, this is

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Root Water Transport Under Abiotic Stress Conditions

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an assumption based in several independent studies, and comprehensive experiments to check this hypothesis are needed. Table 1. Summary of some of the different effects of drought stress and recovery on root hydraulic conductivity (L). Data ordered chronologically

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a

Drought treatment 45d without watering 16d without watering 10h 20% PEGa

Effect on L

Recovery

Plant specie

Reference

Down

Partially

Down

No

UP

Not Checked

Opuntia acanthocarpa Populus tremuloides Oryza sativa

Roots exposed to air during 17h 4d without watering 10d at 75% of field capacity 24h PEGa at 0.35 MPa

Partial increase

Not Checked

Down

No

Down

Partially

Down

Totally

Martre et al. (2001) Siemens and Zwiazek (2003) Lian et al. (2004) Siemens and Zwiazek (2004). Aroca et al. (2006) Aroca et al. (2008) Mahdieh et al. (2008)

Populus tremuloides Phaseolus vulgaris Lactuca sativa Nicotiana tabacum

PEG: Polyethylenglycol.

Although general speaking L decreased under drought stress (see above), the proportion of water circulating by the apoplastic path increases with respect of water circulating by the “cell-to-cell” pathway under drought conditions (Ionenko et al., 2003; Siemens and Zwiazeck 2003). At the same time, several researches have reported a diminution in the expression of root PIP aquaporin genes upon exposure to drought stress (Smart et al., 2001; Jang et al., 2004; Porcel et al., 2006; Aroca et al., 2008; Mahdieh et al., 2008), but the opposite has also been seen (Lian et al., 2004; Aroca et al., 2006), and eventually, the change in expression depends on the PIP gene analyzed (Jang et al., 2004; Aroca et al., 2007; Mahdieh et al., 2008). These results may indicate that each PIP gene has a specific function under drought stress since each gene respond differently to drought and also may regulate the expression of the other PIP gene family members (Jang et al., 2007). For a summary of the effect of drought on PIP gene expression see Table 2. Upon recovery from drought stress, L not always recovers to pre-drought values (Siemens and Zwiazek, 2003; Aroca et al., 2006, 2008), even if in some cases transpiration is fully recovered (Aroca et al., 2006, 2008). These results indicate a possible increase on the water circulating by the apoplastic path. However, in other studies, L recovered totally (Mahdieh et al., 2008) or even showed highest values than pre-drought ones (Zhang et al., 1995). At the same time, PIP gene expression did not recover initial value in some studies (Aroca et al., 2006, 2008), but in others the recovery was total (Mahdieh et al., 2008). Therefore, as happen during drought, L and PIP responses to recovery from drought depend on the plant species studied or on stress intensity.

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Table 2. Summary of some of the effects of drought stress on root PIP expression. Data ordered chronologically Drought treatment 3 to 4d without watering 4 to 48h 250 mM Manitol 2 to 10h with 20% PEG 4d without watering 10d at 70% of field capacity 4d without watering

24h PEG at -0.35 MPa

Effect on PIP Expression Decrease

Plant specie

Reference

Nicotiana glauca

Smart et al. (2001)

9 PIPs decrease, 4 PIPs increase Increase

Arabidopsis thaliana

Jang et al. (2004)

Oryza sativa

Lian et al. (2004)

Increase Decrease

Phaseolus vulgaris Glycine max and Lactuca sativa Phaseolus vulgaris

Aroca et al. (2006) Porcel et al. (2006)

Nicotiana tabacum

Mahdieh et al. (2008)

2 PIPs increase, 1 PIP decrease, 1 PIP not change 2 PIPs decrease, 1 PIP increase

Aroca et al. (2007)

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SALT STRESS EFFECTS ON ROOT WATER UPTAKE Plants under high salt concentration in the soil solution have to solve two main problems. The first problem is the toxicity of solutes. This toxicity is higher when Na+ and Cl- ions are involved. For a review on the toxic effects of salt ions on plants see Ferguson and Grattan (2005). Here we will focus on the second effect that salt stress cause on plant physiology: the osmotic effect, which decrease soil water potential. Similarly to drought stress, salt stress causes a diminution of root water uptake, although when plants are exposed to salt for a long time they retain some capacity to recover their water uptake rate. Under salt conditions toxic ions like Cl- or Na+ are absorbed as well and thus plants need to find equilibrium between the necessity to take up water and the importance to avoid absorption of toxic ions. Salt stress, as well as drought, causes a reduction on the transpiration rate of plants (Gama et al., 2007; Neocleous and Vasilakakis, 2007). However, in some studies, no effect on transpiration rate has been observed (Aroca et al. 2007; Sawas et al., 2007). On the contrary, L decreases in almost all studies due to the high osmotic gradient between soil solution and the inner part of the roots (Martínez-Ballesta et al., 2006). Under salt stress, it has been usually observed a decrease in the expression and abundance of PIP aquaporins genes and proteins (Boursiac et al., 2005; Martínez-Ballesta et al., 2006). Also, Boursiac et al. (2005) found an internalization of plasma membranes containing PIP proteins in Arabidopsis root cells upon exposure to salt. These results could explain the diminution of L under salt stress. However, the above cited experiments were undertaken during a short period of time, no more that 24 h. On the contrary, when salt exposure is prolonged for a week, an enhancement of some PIP gene expression has been observed (Kawasaki et al. 2001; Aroca et al., 2007). In fact, Aroca et al. (2007) found an increase on the root exudation rate in bean

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plants subjected to 50 mM NaCl during one week, when these plants were inoculated with a mycorrhizal fungus. The different response of PIP genes under salt stress depending on the time scale could be explained as follows. Since PIP proteins facilitate the pass of water following an osmotic gradient, it could be beneficial for the plants to reduce their expression in plasma membrane to avoid loss of water under salt stress. However, plants have the capacity to reduce their cell osmotic potential by accumulating different compatible solutes by a process known as osmotic adjustment (Ashraf, 2004). When the osmotic adjustment takes place, it is possible that roots recover the ability to take up water and so they need again aquaporins in the plasma membranes of their cells (Figure 3).

1st Phase

2nd Phase

Soil Solution Osmotic Potential

Root Cell Solutes Accumulation

PIP Root Expression

PIP Root Expression

Water Loss

Root Water Uptake

Figure 3. Scheme summarizing the possible behaviour of root hydraulic properties and PIP aquaporins under salt stress.

COLD STRESS EFFECTS ON ROOT WATER UPTAKE Most crop plants original from tropical regions like maize or tomato are cultivated in temperate regions. Since these plant species belong to warmer regions they suffer several disorders when they are growing in cold areas. One of the effects of cold in plant sensitive species is dehydration of leaf tissues (Pardossi et al., 1992; Aroca et al., 2001). Under low temperature conditions, plant sensitive species keep their stomata open, and are unable to maintain their leaf water status unchanged (Pardossi et al., 1992; Aroca et al., 2001). However, the way the root takes water up under cold conditions is also crucial in keeping leaf water status unchanged. Hence, when two maize genotypes differing in their cold sensitivity

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were subjected to 5 ºC, both of them presented the same transpiration rate, but the tolerant genotype had greater root exudation rate and L than the sensitive one (Aroca et al., 2003b). In fact, recovery from the water deficit caused by cold is associated to the recovery of the capacity of the roots to take water up again in bean plants (Vernieri et al., 2001). Aroca et al. (2005) carried out the first approach at a molecular level dealing with the role of PIP aquaporins on the recovery of root water uptake upon cold treatment in two maize genotypes differing in cold sensitivity. In this research it was found that cold treatment increased the amount of PIP proteins in the roots of both genotypes, but only the tolerant one also increased L. The same behaviour of PIP proteins and L was found when both genotypes were subjected to hydrogen peroxide treatment. Therefore, authors concluded that PIP aquaporins are necessary to recover root water uptake upon cold exposure, but not sufficient. Plants also need to cope with the oxidative damage coupled to cold stress (Figure 4).

Cold

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Initial Decrease of L

Increase PIP Expression

Increase Antioxidant Capacity

L Recovers Adapted from Aroca et al. (2005). Figure 4. Scheme summarizing the possible response of L and PIP aquaporins to cold stress in cold tolerant species.

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FLOODING STRESS EFFECTS ON ROOT WATER UPTAKE Plant flooding stress occurs in soils close to riparian zones or in regions with transitory heavy rains and poor soil drainage (Nicolás et al., 2005; Herrera et al., 2008). Under flooding conditions oxygen molecules are depleted quickly by root and microbial respiration. Hence, root metabolism is altered changing from aerobic respiration to fermentation causing a drop in the cytoplasmic pH (Kulichikhin et al. 2007). This acidification plus other chemical signals from the roots induce stomatal closure and decrease transpiration rate (Ahmed et al., 2006; Else et al., 2006). At the same time root exuded sap flow diminishes together with L (Jackson et al., 2003). However, under certain circumstances, a recovery of L upon flooding has been observed (Herrera et al., 2008). This recovery is due to the transpiration recovery and to the aeration of the roots, caused by changes in its anatomy (Herrera et al., 2008). In an elegant study, Tournaire-Roux et al. (2003) found a close relationship between a decrease of cytosolic pH and a decrease of L in Arabidopsis plants. At the same time, these authors found that a drop of cytosolic pH caused the protonation of a histidine residue of PIP genes, and that this protonation caused, at the same time, a decrease of PIP water transport activity. Although Tournaire-Roux et al. (2003) were focused on flooding stress, a drop of citosolic pH have been also observed in other abiotic stresses like salt in sensitive species (Kader et al., 2007). Therefore, this regulation mechanism of PIP activity could be involved in the reduction of L by other stresses, but it needs to be checked empirically.

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ABSCISIC ACID AND OTHER SIGNALS EFFECTS ON ROOT WATER TRANSPORT Plant response to abiotic stresses is mediated by several molecular signals including different hormones and chemicals. Abscisic acid (ABA) is the most studied plant hormone involved on plant response to abiotic stresses (Hirayama and Shinozaki, 2007; Kim, 2007). At leaf level, it is well known how ABA induces stomatal closure (Wang and Song, 2008). Thus, ABA induces the production of reactive oxygen species and reactive nitrogen species, which stimulate the release of calcium, the activation on anion channels and eventually the efflux of potassium that causes the stomatal closure (Munemasa et al., 2007). However, the signals involved in ABA modification of root hydraulic properties are poorly explored (Aroca, 2006). When ABA is applied exogenously to plants via foliar spraying (Aroca et al. 2006) or dilution into nutrient solution (Aroca et al., 2003; Aroca, 2006), ABA induces (Aroca, 2006; Aroca et al., 2006), has no effect (Wan and Zwiazek, 2001), or reduces (Aroca et al., 2003) L. These discrepancies could be caused by the different plant species used, differences in ABA concentrations applied, or the different environmental conditions. However, the most common effect of ABA is increasing L. Aroca (2006) found that, at certain ABA concentrations (between 1 and 5 μM), exogenous application of catalase (an enzyme that removes H2O2) or ascorbate (a broad range antioxidant) diminished the increase of L mediated by ABA. However, at higher concentrations of ABA, exogenous catalase had the opposite effect. Hence, although a clear conclusion was not possible to establish, it seemed obvious that reactive oxygen species were involved in the effect of ABA on L.

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In apparently opposite studies to that of Aroca (2006), several authors have found that exogenous H2O2 induced a reduction of L (Ktitorova et al., 2002; Rhee et al., 2007). However, in other studies the effect of H2O2 on L depended on the plant tolerance to an oxidative stress (Aroca et al., 2005). Therefore, as it has been pointed out (Miller et al., 2008), H2O2 can have a dual function acting either as a molecular signal or as a damaging agent, depending on its concentration in the plant cells. Other hormone involved in the regulation of plant water relations under abiotic stress conditions is methyl jasmonate (MeJ). In fact, MeJ acts similarly to ABA in closing stomata during abiotic stresses (Munemasa et al., 2007). However, little is known about the effect of MeJ on root water transport properties. Only a study by Lee et al. (1996) deals marginally with the effect of MeJ on root exudation rate in rice, reporting a positive effect. The well known second messenger Ca2+ has also a role on regulating root hydraulic properties under abiotic stress conditions, especially under salt stress. In fact, although under in vitro conditions, Ca2+ ions inhibit aquaporin activity (Gerbeau et al., 2002), it is well known that Ca2+ also alleviates the inhibition of L caused by salt stress (Martínez-Ballesta et al., 2006). Again deeper studies are needed to understand the role of Ca2+ on the regulation of root hydraulic properties under abiotic stress conditions.

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CONCLUSION In the last decade a big effort has been taken to understand how root water transport responded to abiotic stresses, especially to drought and salinity, being other abiotic stresses less studied. It is well established that root water transport is as important as stomata regulation in order to keep plant water status in normal values under abiotic stress conditions. Nevertheless, it still remains unknown how this response is achieved at a molecular level. In fact, although it seems clear that aquaporins should be involved in that response, it is difficult to set a scenary integrating aquaporins and L, most probably due to the size and diversity of plant aquaporins gene family and to the different role of each plant aquaporin in response to each type of abiotic stress. At the same time, we need also to integrate the several molecular signals involved in the response of root hydraulic properties to different abiotic stresses.

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Chapter 4

AMINO ACIDS IN THE RHIZOSPHERE: A REVIEW Rejsek Klement, Formanek Pavel & Vranova Valerie Department of Geology and Soil Science, Faculty of Forestry and Wood Technology, Mendel University of Agriculture and Forestry, 613 00 Brno, Czech Republic

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ABSTRACT Amino acids are of great significance as regards the study of carbon and nitrogen cycling in soil. These nitrogen compounds, released from roots into the soil, provide N for rhizosphere microflora, react with soil components and, in some cases, can be of significance in direct N-nutrition of plants. In contrast to non-proteinaceous amino acids (phytosiderophores), proteinaceous amino acids have a limited role in nutrient mobilization. In general, amino acids are released from roots via passive diffusion, while their re-uptake is an active process. Exudation sites of particular amino acids can differ within the root system, whereas their re-uptake can occur along the whole length of the root. Amino acid exudation and re-uptake, and the net results of these fluxes, can result in either positive or negative levels of individual amino acids. In this chapter, we discuss factors that influence amino acid exudation, including age, defoliation, nutrient deficiency, temperature, light intensity, mycorrhizal colonization, diurnal fluctuations, water-deficit stress, concentration around roots, microorganisms, mechanical impedance, elevated [CO2], microbial metabolites, nitrates and aluminum. Alanine, glutamine, aspartic acid, glycine, serine, glutamic acid, proline, lysine, γ-aminobutyric acid, valine, arginine and cystine are the most abundant amino acids in root exudates of C4 plants. In C3 plants, serine, glycine, glutamic acid, alanine, tyrosine, arginine, proline, cystine and aspartate are most abundant. C4 plants exude more glutamine, lysine, γ-aminobutyric acid and valine, while C3 plants exude more tyrosine.

Keywords: amino acids, rhizosphere, root exudates, C3 and C4 plants, uptake.

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INTRODUCTION Up to 40% of the net carbon fixed during photosynthesis can be transferred into the rhizosphere through so-called “rhizodeposition” (Whipps and Lynch, 1983, 1990). Rhizodeposition is classified as water-soluble root exudates (e.g. sugars, amino acids and organic acids), secretions (polymeric carbohydrates and enzymes), plant mucilages (more complex organic compounds originating in root cells or from bacterial degradation), mucigel (a gelatinous layer composed of intermixed mucilages and soil particles), and lysates such as the content of sloughed-off cells, cell walls or whole roots (Brady, 1990). Rhizodeposition has a diverse range of functions in plant nutrition and soil ecology. Some compounds are able to improve nutrient availability, e.g. phytosiderophores increase availability of Fe or Zn and citric acid acts on P-mobilization (von Wirén et al., 1993; Norvell et al., 1993; Zhang, 1993; Gerke, 1994; Staunton and Leprince, 1996; Schilling et al., 1998), while others can relieve Al-toxicity by chelating this phytotoxic metal, act as allelochemicals, serve as signaling substances for the establishment of symbiotic relationships between plant roots and microorganisms, or serve as an important carbon and energy source for rhizosphere soil microorganisms (Neumann and Römheld, 2007). Exudation of amino acids from plant roots is of great significance for carbon and nitrogen cycling in soil, as nitrogen compounds released from roots into the soil provide N for rhizosphere microflora (Grayston et al., 1998) and for neighboring plants (Høgh-Jensen and Schjoerring, 2001; Jones et al., 2005). Amino acids, which are readily degradable by soil microorganisms, are usually the third (or second) most abundant compounds in water-soluble root exudates and have been the subject of many studies (e.g. Mench, 1985; Merbach et al., 1999; Gransee and Wittenmayer, 2000). Knowing the amount of amino acid in the rhizosphere is important, as the relative proportion of amino acids to sugars affects the relative amount of C and N available for microbial growth. The composition of root exudates influences the colonization of the rhizosphere by microorganisms. So-called phytoeffective microorganisms (e.g. Pseudomonas or Serratia) are of especial interest as regards the nutrition and growth of plants. For example, addition of the amino acid fraction of root exudates from N-deficient wheat led to stronger Serratia-induced N-acquisition, as reported by Merbach et al. (1999). Nitrogenous compounds, including amino acids released from roots, may provide nitrogen for neighboring non-N2-fixing plants. Exudation of nitrogen from roots by a donor plant, and its reabsorption by a receiver plant, provides one of the mechanisms for interplant short-term N transfer (Paynel et al., 2001). Root exudates released into the soil are decomposed by microorganisms, which stimulates decomposition of the native soil organic matter and allows some of their components to be incorporated into the more stable fraction of the soil (Vancura, 1988). The amount of amino acid in the rhizosphere results from fluxes between the soil, microorganisms and plant roots. The significance of amino acid exudation by plants, however, remains unclear. Rhizodeposition may enhance both denitrification and N immobilization in the rhizosphere (Qian et al., 1997). Free-living nitrogen-fixing bacteria in the rhizosphere of the coast Douglas-fir (Pseudotsuga menziesii) release amino acids, enhancing ectomycorrhizal formation (Li and Hung, 1987). Many rhizosphere organisms have chromosomally encoded low affinity chemotaxis to the host plant carbohydrates and amino acids, eliciting chemotaxis to the host (Gaworzewska and Carlile, 1982). Mycorrhiza

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fungi increase the availability of organic nitrogenous compounds in the rhizosphere (e.g. proteins and amino acids) by releasing proteases (Abuzinadah and Read, 1988). Vergnaud et al. (1987) reported that heat treatment of root exudates of common alder (Alnus glutinosa) prevented root hair deformation and subsequent Frankia infection, suggesting that proteins in root exudates are involved in the symbiotic process; the identification of these proteins and their role in the symbiosis remain unknown. The following amino compounds have been found in root exudates from various plants: α - and β-alanine, α-amino adipic acid, γ-amino butyric acid, α-amino butyric acid, α-amino-γhydroxypimelic acid, arginine, asparagine, aspartic acid, citrulline, cystathionine, cysteine, cystine, cysteic acid, homocysteic acid, deoxymugineic acid, 3-epihydroxymugineic acid, βpyrozolyalanine, uracylalanine, pipecolic acid, phosphoserine, phosphoethanolamine, glutamine, glutamic acid, glycine, methionine sulfoxide, homoserine, histidine, isoleucine, leucine, lysine, methionine, mugineic acid, ornithine, phenylalanine, proline, serine, threonine, tyrosine, valine and derivatives of phenylalanine and phenylglycine (Vancura and Garcia, 1969; Vancura, 1988; Ofosu-Budu et al., 1990; Grayston et al., 1996; Uren, 2007). Certain amino acids are necessary for phytohormonal action of rhizosphere microflora, such as L-tryptophan, the main source of which is root exudates in the rhizosphere. Some rhizosphere microflora can use this compound as a precursor for the biosynthesis of indole-3acetic acid (Kravchenko et al., 2004). Proteinaceous amino acids have a limited role in nutrient mobilization (Jones and Darrah, 1994). On the other hand, non-proteinaceous amino acids (phytosiderophores) are important in the mobilization of plant nutrients. Gries et al. (1998) found induced exudation of a phytosiderophore, identified as desoxymugineic acid, by roots of wood barley (Hordelymus europaeus (L.) under conditions of Fe- and Cu-deficiency. Exudation of this compound was not induced, however, in cases of Zn- or Mn-deficiency. The problems associated with phytosiderophores have been well described in the works of, for example, Dakora and Phillips (2002) or Crowley and Kraemer (2007).

MECHANISM OF AMINO ACID EXUDATION, NET AMINO ACID EXUDATION (EFFLUX) Plants naturally cycle amino acids across root cell plasma membranes, and any net efflux is termed exudation. The mechanisms of exudation of amino acids and other substances of low molecular weight are described in the work of Neumann and Römheld (2007). It has been suggested that root exudation of amino acids generally occurs via passive diffusion (Shepherd and Davies, 1994; Jones and Darrah, 1994; Rroço et al., 2002) and may be enhanced by stress factors affecting membrane integrity, such as nutrient deficiency (e.g. of K, P, Zn), temperature extremes or oxidative stress (Cakmak and Marschner, 1988; Rovira, 1969; Ratnayake et al., 1978; Schwab et al., 1983). The quantity of amino acids released will be related to the concentration gradient between the plant roots and the rhizosphere, the reabsorption of amino acids exuded by plant roots, and uptake through bacterial consumption (Shepherd and Davies, 1994). According to Jones and Darrah (1994), most of the amino acids exuded from plant roots are recaptured through an active transport mechanism. Uptake of amino acids by root cells involves proton-pumping ATPases that maintain an electrochemical

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potential difference across the plasma membrane to support uptake into the plant by protoncoupled amino-acid transporters (Farrar et al., 2003). Thus, amino-acid exudation is more properly viewed as net efflux. Efflux of amino acids from plant roots can be determined separately by blocking reabsorption of amino acids with carbonyl cyanide m-chlorophenylhydrazone (see Phillips et al., 2006). Although there have been few studies on the regulation of root transporters involved in exudate recapture, the transport systems appear to be constitutively expressed in corn seedling roots and not down-regulated by the presence of inorganic N (Jones and Darrah, 1994; Bhattacharya et al., 2002), while amino acid uptake is repressed by NH4+ in Scots pine Pinus sylvestris L. (Persson and Nashölm, 2002).

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LOCATION OF AMINO ACID EXUDATION AND RE-UPTAKE The exudation sites for various compounds differ within the root system. Frenzel (1960) found that root tips of sunflowers (Helianthus annuus) exuded threonine and asparagine, whereas root hairs of the same plant exuded leucine, valine, phenylalanine and glutamic acid. Jones and Darrah (1994) deduced from root concentration gradients that the main site of amino acid exudation was at the root tips. According to Catska (1965), amino acids were exuded particularly in the zone of root elongation, whereas sugars and organic acids were exuded from the basal parts of roots. Pearson and Parkinson (1961) found that the region behind the root tip of the broad bean (Vicia faba) released ninhydrin-reacting material but no such release was detected in older parts of the roots. Schroth and Snyder (1961) found that bean seedlings mainly exuded amino acids from the elongating roots (primary, lateral and adventitious) and no exudates were detected from the older parts of roots. Jaeger et al. (1999) reported the highest concentration of tryptophan at 12–16 cm from the root tip of an annual grass Avena barbata. Perforation of the epidermis by lateral roots in older sections may allow the release of a portion of the amino acids. It is also possible that more amino acids are synthesized in the mature portions of roots, that amino acids synthesized in root tips are immediately incorporated into new tissue, and that amino acids in mature parts of roots may persist longer and be subject to leakage through lateral root channels (Jaeger et al., 1999). From a limited range of crop plant studies, it appears that exudate recapture can occur along the entire length of the root and that the transporter kinetics for exudates are similar to those for inorganic nutrients (Jones and Darrah, 1994, 1996; Barber, 1995) and those of the soil microorganisms with which the plants are presumably in competition (Jones and Hodge, 1999). In soil, physical and chemical adsorptive forces could prevent amino acid reabsorption by the plant (Jones and Darrah, 1994) and ensure that microorganisms obtain significant amounts, either by competitive uptake (Owen and Jones, 2001) or by active disruption of fluxes.

FACTORS INFLUENCING AMINO ACID EXUDATION In general, the relative and absolute amount of compounds in water-soluble root exudates varies with the plant species, cultivar, the plant’s age, environmental conditions (including light intensity and temperature), the nutritional status of the plants, activity of retrieval

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mechanisms, various stress factors, herbicides, mechanical impedance, soil characteristics and activity of microorganisms in the rhizosphere (Bartels and Weier, 1965; Rovira, 1969; Hale et al., 1971; Hale et al., 1978; Rovira and Davey, 1974; Martin, 1977; Hale and Moore, 1979; Ferguson and Menge, 1982; Boeuf-Tremblay et al., 1995; Paynel et al., 2001; Neumann and Römheld, 2007). According to Smith (1976), mature sugar maple trees (Acer saccharum) exuded higher amounts of amino acids, amides and organic acids as compared to seedlings. Shepherd and Davies (1994) reported that proportions of alanine, γ-amino butyric acid, glutamic acid and isoleucine in root exudates increased as the plant aged, that older plants released more amino acid per plant while younger plants released more amino acid per gram root dry weight, and that amino acid composition and concentration in collection medium was dependent on experimental set up and, more specifically, on the presence or absence of sterile conditions. Bacilio-Jiménez et al. (2003) found that the amount of amino acid residue in hydrolyzed root exudates of axenically grown rice (Oryza sativa) was highest in the first week, and decreased by more than 50% between the first and second weeks, though it was still significantly higher in week 2 than in weeks 3 and 4. In the first week of cultivation, 16 individual amino acids were detected whereas only 15 and 12 were detected during the third and fourth weeks, respectively. Shepherd and Davies (1994) reported highest ratios between consumption of amino acids by microorganisms and exudation from the roots of forage rape for asparagine, arginine, glutamic acid, glutamine and lysine, suggesting that a degree of selectivity exists for glutamic acid and nitrogen-rich acids on the part of the consuming microorganisms. Bowen (1969) reported that Monterey pine (Pinus radiata) seedlings growing in conditions of N-deficiency exuded less asparagine, glutamine, glycine and all other amino acids than seedlings in nutrient sufficient conditions. The same seedlings grown under P-deficient conditions exuded more amino N than those in nutrient sufficient conditions. Increased temperature has been shown to increase the amount of exudate and the relative proportions of amino acids exuded by tomato (Lycopersicon esculentum) and white clover (Trifolium repens). The level of soluble amino acid in root exudates has been found to change with alterations in light intensity (Ferguson and Menge, 1982). Smith (1972) showed that defoliation influenced exudation of amino acids by sugar maple, with defoliated trees exuding greater amounts of cystine, lysine, glutamine, tyrosine and phenylalanine, and non-defoliated trees exuding larger amounts of glycine, homoserine, methionine and threonine. Mycorrhizal colonization of roots also influences amino acid exudation. For example, Leyval and Berthelin (1993) found increased amounts of amino acids in the mycorrhizal (Lacaria laccata) rhizosphere of common beech (Fagus sylvatica), as compared with nonmycorrhizal plants. Cliquet et al. (1997) found no significant differences in the amino acid composition of root zone solutions from plants with and without the arbuscular mycorrhizal fungus, although the amino acid profiles and quantities could be influenced by type of N-nutrition. Ferguson and Menge (1982) reported that the level of soluble amino acids in root exudates of 2-month old Sudan grass (Sorghum vulgare var. sudanense) plants was not correlated with the production of spores from the vesicular-arbuscular mycorrhizal fungi Glomus fasciculatus. The exudation rate of amino acids has been shown to fluctuate diurnally, with exudation much reduced during the dark period (Richter et al., 1968). Large differences were noted in peptide concentrations in night- and day-rhizodeposits of sandy soil planted with corn (Zea mays L.) (Melnitchouck et al., 2005). Ofosu-Budu et al. (1990) noted that the maximum nitrogen excretion rate of the soybean (Glycine max L.) was recorded in

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daytime during the vegetative and flowering stages but at night during the pod-filling stage. Svenningsson et al. (1990) found no statistically significant effects of water-deficit stress on exudation of amino acids from roots of oilseed rape (Brassica napus), stressed plants tended to release smaller amounts of amino acids per unit root dry weight than the control plants (543 and 982 μg . g-1 root dry weight, respectively) and a significantly lower proportion of the exuded dissolved organic carbon was made up of amino acids in the stressed plants as compared with the control (7% as opposed to 27%). Reversible wilting of millet plants (Panicum miliaceum L.) did not change the exudation of some amino acids, such as the basic amino acids, amides, cysteic acid, homocysteic acid, aspartic acid, serine and glycine, but it caused a substantial increase in exudation of glutamic acid, α-alanine, valine and leucine/isoleucine (Vancura and Garcia, 1969).Shepherd and Davies (1994) reported that the release of amino acids into a fixed volume of collection medium was concentration-limited, giving rise to similar convex accumulation profiles for individual acids. In contrast, amino acid accumulation in a continuously circulating collection medium was not concentrationlimited, showing a linear accumulation pattern. Application of P to foliage, in the form of sodium phosphate, reduces amino acid exudation and increases sugar exudation from roots (Balasubramanian and Rangaswami, 1973). Barber and Gunn (1974) observed that exudation of amino acids was increased when roots were grown through a solid medium. Phillips et al. (2006), during experiments with elevated levels of [CO2], recorded a significant increase (P