Endophytes: Mineral Nutrient Management [3, 1 ed.] 303065446X, 9783030654467

Table of contents :
Preface
Contents
Contributors
Part IEndophytes in Agriculture
1 Endophytes in Mineral Nutrient Management: Introduction
1.1 Introduction
1.2 Frontiers of Endophyte
1.2.1 Avenues in Pharmaceuticals
1.2.2 Fungal Endophytes
1.2.3 Spore Bearing Endophyte Enhancing Plant Nutrient Uptake
1.2.4 Endophyte for Crop Protection
1.2.5 Phosphorus Management by Endophytes
1.2.6 Endophytes: Ecological Advances
1.2.7 PGPB: Nutrient Use Efficiency
1.2.8 Iron Management: Endophytes in Siderophore Production
1.2.9 Endophyte: Biotechnology and Bioinformatics
1.3 Conclusions
References
2 Bioefficacy of Endophytes in the Control of Plant Diseases
2.1 Introduction
2.2 Bacterial Endophytes as BCAs
2.2.1 Antagonism
2.2.2 Induction Disease Resistance in Plants
2.2.3 Parasitism
2.3 Fungal Endophytes
2.3.1 Clavicipitaceous Fungal Endophytes (Grass-Endophytes Interactions)
2.3.2 Non-Clavicipitaceous Fungal Endophytes
2.3.3 Mechanisms of Biological Control by Fungal Endophytes
2.4 The Relation Between Nutrient Management and Biological Control
2.5 Conclusions
References
3 Microbial Endophytes: Sustainable Approach for Managing Phosphorus Deficiency in Agricultural Soils
3.1 Introduction
3.2 Phosphorus Availability in Soil
3.3 Colonization of Endophytic Microbes in Tissues
3.3.1 Rhizosphere and Root Colonization
3.3.2 Colonization of Aerial Plant Tissues
3.4 Occurrence and Diversity of Bacterial Endophytes
3.5 Phosphorus Solubilization by Endophytic Microorganisms
3.5.1 Phosphate Solubilization by Endophytic Bacteria
3.5.2 Phosphate Solubilization by Endophytic Fungi
3.6 Beneficial Traits of Endophytic Microorganisms
3.6.1 Nitrogen Fixation by Endophytes
3.6.2 Phytohormone
3.6.3 Endophytic Microbes as a Biocontrol Agent
3.6.4 Endophytes in ACC Deaminase and Stress Amelioration
3.6.5 Metals Solubilization by Endophytes
3.7 Inoculation Responses of Endophytes on Plants
3.8 The Genetics Involved in Endophytic Behavior and Phosphate Solubilization
3.9 Conclusion
References
4 Cattle Dung Manure Microbiota as a Substitute for Mineral Nutrients and Growth Management Practices in Plants
4.1 Introduction
4.2 Microbiology of Dung
4.3 Dung: Bioresource of Energy
4.4 Dung: Source of Industrial Products
4.5 Dung and the Mineral Nutrients Management
4.6 Dung on Nutrient Uptake in Plants
4.7 Dung Applications: Success and Bottleneck
4.8 Effect of the Blending of Organic and Inorganic Fertilizers
4.9 Dung in Agrobiological Practices
References
5 Fluorescent Pseudomonads in Iron Chelation and Plant Growth Promotion in Abiotic Stresses
5.1 Introduction
5.2 Interaction Between Deleterious Rhizo Bacteria (DRB) and PGPR
5.3 Iron Deficiency and Siderophore Production
5.4 Siderophores
5.5 Plant Responses to Salinity
5.6 Unavailability of Iron in Saline Soils
5.7 Avoidance of Iron Limitation in Saline Soils
5.8 Fluorescent Pseudomonads—A Sustainable Solution for Iron Limitation in Saline Soils
5.9 Root Colonization and Plant Growth Promotion
5.10 Effect of Iron and PH Levels
5.11 Effect of Iron on Antagonism
5.12 Influence of Amino Acids, Organic Acids, and Sugars on Growth, Fluorescence, and Siderophore Production
5.13 Siderophores as Iron Storage Compounds
5.14 Conclusion and Future Aspects
References
Part IIEndophytes and Mineral Nutrition
6 Microbial Endophytes: New Direction to Natural Sources
6.1 Introduction
6.2 What Is Endophyte?
6.3 Classification of Endophytic Fungi
6.4 Plant Defense Responses in Relation to Endophyte-Pathogen and Host Plant
6.5 Plant Growth Stimulating Endophytic Bacteria
6.6 Biodiversity of Bacterial Endophytes
6.7 Interactions of Endophytes and the Host Plant
6.8 Endophytes and Abiotic Stresses
6.9 Antimicrobial Activity of Endophytes
6.10 Endophytic Bioactive Alkaloids
6.11 Endophytes in Agriculture and Medicine: Future Prospects
References
7 Tropical Endophytic Bacillus Species Enhance Plant Growth and Nutrient Uptake in Cereals
7.1 Introduction
7.2 Plant Colonizing Endophytic Bacteria
7.3 Endophytic Bacillus and Plant Growth Promotion in Tropical Soils
7.4 Bacillus in Post-Genomic Era
7.5 Commercialization and Challenge of Bacillus Biotechnological Products
7.6 Conclusion and Future Prospects
References
8 Biotechnology and Bioinformatics of Endophytes in Biocontrol, Bioremediation, and Plant Growth Promotion
8.1 Introduction
8.2 Definition of Endophytes
8.3 Endophytes Ongoing Researches and Major Trends
8.4 Endophyte Taxonomic Affinities
8.5 Endophyte Lifestyle
8.6 Plant Growth-Promoting Mechanisms
8.6.1 Atmospheric Nitrogen Fixation
8.6.2 Phosphorus Solubilization
8.6.3 Siderophore Production
8.6.4 Phytohormones Synthesis and Regulation
8.6.5 Production of Cell Wall-Degrading Enzymes
8.6.6 Hydrogen Cyanide Production (HCN)
8.6.7 Volatile Organic Compounds (VOCs)
8.6.8 Competition for Space and Nutrients
8.6.9 Antibiosis and Antibiotics
8.6.10 Detoxification and Degradation of Pathogens Virulence Factors
8.6.11 Induced Systemic Resistance (ISR)
8.7 Biological Applications of Endophytic Microorganisms
8.8 Omic Approaches for Endophytes
8.9 Conclusion and Prospects
References
9 Phosphate Solubilization by Endophytes from the Tropical Plants
9.1 Introduction
9.2 Phosphorus Solubilization by Microorganisms
9.3 Endophytic Microorganisms: A Way to Reduce the Application of Agrochemicals in Agrobiology Systems
9.4 Endophytic Bacteria from Tropical Plants of Economic Importance: Phosphorus Solubilization Potential
9.4.1 Endophytic Bacteria from Coffea arabica
9.4.2 Endophytic Bacteria from Jatropha curcas
9.4.3 Plant Growth-Promoting Potential of Phosphate Solubilization by Endophytic Bacteria Isolated from Tropical Mangrove Forests
9.4.4 The Agronomic Potential of Phosphate Solubilization by Endophytic Fungi from the Tropical Savanna
9.5 Conclusion
References
Part IIIBeneficial Microbes and Mineral Nutrient Management
10 Endophytic Actinobacteria Associated with Mycorrhizal Spores and Their Benefits to Plant Growth
10.1 Introduction
10.2 Endophytic Actinobacteria from Mycorrhiza
10.3 Plant Growth-Promoting (PGP) Activities of Endophytic Actinobacteria
10.3.1 Endophytic Actinobacteria Associated with Nutrient Uptake in Plants
10.3.2 Biocontrol Activities of Endophytic Actinobacteria
10.3.3 Phytohormone Production by Endophytic Actinobacteria
10.4 Beneficial Effects of Endophytic Actinobacteria on Plant
10.5 Conclusions
References
11 Endophytes as Plant Nutrient Uptake-Promoter in Plants
11.1 Introduction
11.2 Enhancing Plant Nutrient Uptake
11.3 Endophytes Mediated Mechanisms of Action to Enhance Nutrients Uptake
11.4 Plant Growth Under Alleviation of Stress Conditions
11.5 Conclusion
References
12 Endophytic Rhizobacteria for Mineral Nutrients Acquisition in Plants: Possible Functions and Ecological Advantages
12.1 Introduction
12.2 Putative Functions of Endophytic PGPR for Mineral Nutrients Acquisition in Plants
12.2.1 Endophytic Rhizobacteria and Nitrogen Acquisition in Plants
12.2.2 Endophytic Rhizobacteria and Potassium Acquisition in Plants
12.2.3 Endophytic Rhizobacteria and Phosphorus Acquisition in Plants
12.2.4 Endophytic Rhizobacteria in Zinc Acquisition in Plants
12.2.5 Endophytic Rhizobacteria and Iron Acquisition in Plants
12.3 Ecological Significance of Endophytes in Mineral Nutrients Acquisition by Plants
12.4 Conclusions and Future Prospects
References
13 Plant Growth-Promoting Bacteria: Effective Tools for Increasing Nutrient Use Efficiency and Yield of Crops
13.1 Introduction
13.1.1 Organic Manures: An Alternative Source of Plant Nutrients
13.2 Plant Growth-Promoting Bacteria
13.2.1 Potential Role of Microbes in Nutrient Availability
13.2.2 Nutrient Use Efficiency (NUE)
13.2.3 PGPRs in NUE Enhancement
13.3 Impact on Crop Yield Enhancement
13.4 Conclusion
References
14 Siderophore in Plant Nutritional Management: Role of Endophytic Bacteria
14.1 Introduction
14.2 Types of Siderophore
14.3 Shuttling Mechanism Through Siderophore Mediated Iron Transporter System
14.4 Cell Membrane Siderophore Receptors
14.5 Channel of Fe Transportation in Microbes and Plants
14.6 Approaches Use in Fe and Zn Acquisition by Plants
14.7 Occupations of Siderophore-PGPR in Crop Field
14.8 Conclusion
References
15 Conclusion
References
Index

Citation preview

Sustainable Development and Biodiversity 26

Dinesh Kumar Maheshwari Shrivardhan Dheeman   Editors

Endophytes: Mineral Nutrient Management, Volume 3 123

Sustainable Development and Biodiversity Volume 26

Series Editor Kishan Gopal Ramawat, Botany Department, Mohanlal Sukhadia University, Udaipur, India

This book series provides complete, comprehensive and broad subject based reviews about existing biodiversity of different habitats and conservation strategies in the framework of different technologies, ecosystem diversity, and genetic diversity. The ways by which these resources are used with sustainable management and replenishment are also dealt with. The topics of interest include but are not restricted only to sustainable development of various ecosystems and conservation of hotspots, traditional methods and role of local people, threatened and endangered species, global climate change and effect on biodiversity, invasive species, impact of various activities on biodiversity, biodiversity conservation in sustaining livelihoods and reducing poverty, and technologies available and required. The books in this series will be useful to botanists, environmentalists, marine biologists, policy makers, conservationists, and NGOs working for environment protection.

More information about this series at http://www.springer.com/series/11920

Dinesh Kumar Maheshwari · Shrivardhan Dheeman Editors

Endophytes: Mineral Nutrient Management, Volume 3

Editors Dinesh Kumar Maheshwari Department of Botany and Microbiology Gurukula Kangri Vishwavidyalaya Haridwar, Uttarakhand, India

Shrivardhan Dheeman Department of Microbiology Sardar Bhagwan Singh University Dehradun, India

ISSN 2352-474X ISSN 2352-4758 (electronic) Sustainable Development and Biodiversity ISBN 978-3-030-65446-7 ISBN 978-3-030-65447-4 (eBook) https://doi.org/10.1007/978-3-030-65447-4 © Springer Nature Switzerland AG 2021 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Preface

The present book entitled Endophytes: Mineral Nutrient Management, Volume 3 is in continuation of two previous volumes published on endophytes, their biology, biodiversity, crop productivity, and their role in crop protection. Based on the idea that endophytic microbes are far stronger than the other bacteria in the rhizospheric microbial world, scientists are paying great attention to the understanding of the beneficial nature of endophytes in particular as they bear enormous potentialities for boosting the sustainable growth of crops and agroecosystems. This book is a comprehensive collection of reviews on current science and evidence of biofertilizer ability of endophytes for nutrient management. Some chapter on the endophytic lifestyle in the plant tissues is an attraction of the book. There is an elaborated account of their special traits like competence, root colonization, and/or endophytic phytohormone secretion which act for plant protection and stress sequestration. Entirely, the synergism of practical and theoretical wisdom on endophytes makes this book alive. An elaborated content has also been available in the book on the science of enhancement of nutrient utilization efficiency. Endophytes increase the availability of important nutrients to enrich soil fertility and fulfill the nutritional demand of plants. Further, plant-endophyte interaction evidences a mutual alleviation of biotic and abiotic stresses in diverse habitat and agroclimatic conditions. Genomic tools and techniques can further identify endophytes with the ability of mineral nutrient management which can be utilized in the production of microbial inoculants for future farming. The book presented under the series “Sustainable development and biodiversity” is entirely dedicated to various endophytic genera, able to mineralize micro and macronutrients in the soil and rhizosphere. This book will not only benefit the scientific diaspora but also to the teachers, researchers, graduation and postgraduation students in various streams of life sciences such as Agriculture, Horticulture, Biotechnology, Microbiology, Phytopathology, Agronomy, and Environmental Sciences. We desire to pay our thanks to all the subject specialists and contributors, who lent their cooperation and patience in the completion of this book. Our research team members, who generously assisted in the compilation and completion of this task also deserve a big thanks. We v

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Preface

extend our sincere thanks to Dr. Ineke and her colleagues for their valuable support in the completion of this project. Support from MHRD UGC—BSR is also duly acknowledged. Haridwar, Uttarakhand, India August 2020

Dinesh Kumar Maheshwari Shrivardhan Dheeman

Contents

Part I

Endophytes in Agriculture

1

Endophytes in Mineral Nutrient Management: Introduction . . . . . . Dinesh Kumar Maheshwari and Shrivardhan Dheeman

3

2

Bioefficacy of Endophytes in the Control of Plant Diseases . . . . . . . . Fernando Matias Romero, Amira Susana Nieva, Oscar Adolfo Ruiz, Andrés Gárriz, and Franco Rubén Rossi

11

3

Microbial Endophytes: Sustainable Approach for Managing Phosphorus Deficiency in Agricultural Soils . . . . . . . . . . . . . . . . . . . . . Anupma Dahiya, Rakesh Kumar, and Satyavir S. Sindhu

4

5

Cattle Dung Manure Microbiota as a Substitute for Mineral Nutrients and Growth Management Practices in Plants . . . . . . . . . . . Sandhya Dhiman, Sandeep Kumar, Nitin Baliyan, Shrivardhan Dheeman, and Dinesh Kumar Maheshwari

35

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Fluorescent Pseudomonads in Iron Chelation and Plant Growth Promotion in Abiotic Stresses . . . . . . . . . . . . . . . . . . . . . . . . . . . 105 C. Dileep, C. G. Sreekala, T. S. Reshma, and Surabhi Sankar

Part II

Endophytes and Mineral Nutrition

6

Microbial Endophytes: New Direction to Natural Sources . . . . . . . . . 123 Azim Ghasemnezhad, Arezou Frouzy, Mansour Ghorbanpour, and Omid Sohrabi

7

Tropical Endophytic Bacillus Species Enhance Plant Growth and Nutrient Uptake in Cereals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157 Camila Cristina Vieira Velloso, Vitória Palhares Ribeiro, Chainheny Gomes de Carvalho, Christiane Abreu de Oliveira, Ubiraci Gomes de Paula Lana, Ivanildo Evódio Marriel, Sylvia Morais de Sousa, and Eliane Aparecida Gomes

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Contents

8

Biotechnology and Bioinformatics of Endophytes in Biocontrol, Bioremediation, and Plant Growth Promotion . . . . . . 181 Houda Ben Slama, Hafsa Cherif-Silini, Ali Chenari Bouket, Allaoua Silini, Faizah N. Alenezi, Lenka Luptakova, Armelle Vallat, and Lassaad Belbahri

9

Phosphate Solubilization by Endophytes from the Tropical Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207 Paulo Teixeira Lacava, Paula Cristiane Machado, and Paulo Henrique Marques de Andrade

Part III Beneficial Microbes and Mineral Nutrient Management 10 Endophytic Actinobacteria Associated with Mycorrhizal Spores and Their Benefits to Plant Growth . . . . . . . . . . . . . . . . . . . . . . 229 Krisana Lasudee, Pharada Rangseekaew, and Wasu Pathom-aree 11 Endophytes as Plant Nutrient Uptake-Promoter in Plants . . . . . . . . . 247 Carlos García-Latorre, Sara Rodrigo, and Oscar Santamaría 12 Endophytic Rhizobacteria for Mineral Nutrients Acquisition in Plants: Possible Functions and Ecological Advantages . . . . . . . . . . 267 Becky Nancy Aloo, Vishal Tripathi, Ernest R. Mbega, and Billy A. Makumba 13 Plant Growth-Promoting Bacteria: Effective Tools for Increasing Nutrient Use Efficiency and Yield of Crops . . . . . . . . . 293 Chitra Pandey, Shrivardhan Dheeman, Deepti Prabha, Yogesh Kumar Negi, and Dinesh Kumar Maheshwari 14 Siderophore in Plant Nutritional Management: Role of Endophytic Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315 Gunjan Garg, Sandeep Kumar, and S. Bhati 15 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 Dinesh Kumar Maheshwari Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335

Contributors

Faizah N. Alenezi Environmental Technology and Management Department, College of Life Sciences, Kuwait University, Kuwait City, Kuwait Becky Nancy Aloo Department of Sustainable Agriculture and Biodiversity Conservation, Nelson Mandela African Institution of Science and Technology, Arusha, Tanzania; Department of Biological Sciences, University of Eldoret, Eldoret, Kenya Paulo Henrique Marques de Andrade Laboratory of Microbiology and Biomolecules – LaMiB, Department of Morphology and Pathology, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, SP, Brazil; Evolutionary Genetics and Molecular Biology Graduation Program – PPGGEv, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, SP, Brazil Nitin Baliyan Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India Lassaad Belbahri NextBiotech, Agareb, Tunisia; Laboratory of Soil Biology, University of Neuchatel, Neuchatel, Switzerland S. Bhati School of Biotechnology, Gautam Buddha University, Greater Noida, Uttar Pradesh, India Ali Chenari Bouket Plant Protection Research Department, East Azarbaijan Agricultural and Natural Resources Research and Education Center, AREEO, Tabriz, Iran Chainheny Gomes de Carvalho Centro (UNIFEMM), Sete Lagoas, MG, Brazil

Universitário

de

Sete

Lagoas

Hafsa Cherif-Silini Laboratory of Applied Microbiology, Department of Microbiology, Faculty of Natural and Life Sciences, University Ferhat Abbas Setif-1, Setif, Algeria ix

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Contributors

Anupma Dahiya Department of Microbiology, CCS Haryana Agricultural University, Hisar, India Shrivardhan Dheeman Department of Microbiology, School of Life Sciences, Sardar Bhagwan Singh University, Balawala, Dehardun, India; Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India Sandhya Dhiman Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India C. Dileep Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Alappuzha, Kerala, India Arezou Frouzy Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran Carlos García-Latorre School of Agricultural Engineering. Institute of Dehesa Research, University of Extremadura, Badajoz, Spain Gunjan Garg School of Biotechnology, Gautam Buddha University, Greater Noida, Uttar Pradesh, India Andrés Gárriz Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Azim Ghasemnezhad Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran Mansour Ghorbanpour Department of Medicinal Plants, Faculty of Agriculture and Natural Resources, Arak University, Arak, Iran Eliane Aparecida Gomes Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil Rakesh Kumar Department of Microbiology, CCS Haryana Agricultural University, Hisar, India Sandeep Kumar Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India Paulo Teixeira Lacava Laboratory of Microbiology and Biomolecules – LaMiB, Department of Morphology and Pathology, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, SP, Brazil; Biotechnology Graduation Program – PPGBiotec, Center of Exact Sciences and Technology, Federal University of São Carlos, São Carlos, SP, Brazil; Evolutionary Genetics and Molecular Biology Graduation Program – PPGGEv, Center for Biological and Health Sciences, Federal University of São Carlos, São Carlos, SP, Brazil Krisana Lasudee Microbiology Section, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand

Contributors

xi

Lenka Luptakova Department of Biology and Genetics, Institute of Biology, Zoology and Radiobiology, University of Veterinary Medicine and Pharmacy, Kosice, Slovakia Paula Cristiane Machado Biotechnology Graduation Program – PPGBiotec, Center of Exact Sciences and Technology, Federal University of São Carlos, São Carlos, SP, Brazil Dinesh Kumar Maheshwari Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India Billy A. Makumba Department of Biological Sciences, Moi University, Eldoret, Kenya Ivanildo Evódio Marriel Universidade Federal de São João Del-Rei (UFSJ), São João del-Rei-MG, MG, Brazil; Centro Universitário de Sete Lagoas (UNIFEMM), Sete Lagoas, MG, Brazil; Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil Ernest R. Mbega Department of Sustainable Agriculture and Biodiversity Conservation, Nelson Mandela African Institution of Science and Technology, Arusha, Tanzania Yogesh Kumar Negi Department of Basic Sciences, College of Forestry (VCSG UUHF), Ranichauri, Tehri Garhwal, Uttarakhand, India Amira Susana Nieva Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Christiane Abreu de Oliveira Centro Universitário de Sete Lagoas (UNIFEMM), Av. Marechal Castelo Branco, Sete Lagoas, MG, Brazil; Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil Chitra Pandey Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala, India Wasu Pathom-aree Research Center of Microbial Diversity and Sustainable Utilization, Microbiology Section, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand Ubiraci Gomes de Paula Lana Centro Universitário de Sete Lagoas (UNIFEMM), Av. Marechal Castelo Branco, Sete Lagoas, MG, Brazil; Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil Deepti Prabha Department of Seed Science and Technology, Chauras Campus, HNB Garhwal University, Srinagar, Uttarakhand, India Pharada Rangseekaew Microbiology Section, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand

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Contributors

T. S. Reshma Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Alappuzha, Kerala, India Vitória Palhares Ribeiro Universidade Federal de São João Del-Rei (UFSJ), São João del-Rei-MG, MG, Brazil Sara Rodrigo School of Agricultural Engineering. Institute of Dehesa Research, University of Extremadura, Badajoz, Spain Fernando Matias Romero Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Franco Rubén Rossi Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Oscar Adolfo Ruiz Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina Surabhi Sankar Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Alappuzha, Kerala, India Oscar Santamaría Department of Construction and Agronomy, University of Salamanca, Zamora, Spain Allaoua Silini Laboratory of Applied Microbiology, Department of Microbiology, Faculty of Natural and Life Sciences, University Ferhat Abbas Setif-1, Setif, Algeria Satyavir S. Sindhu Department of Microbiology, CCS Haryana Agricultural University, Hisar, India Houda Ben Slama NextBiotech, Agareb, Tunisia Omid Sohrabi Department of Horticultural Sciences, Guilan University, Rasht, Iran Sylvia Morais de Sousa Universidade Federal de São João Del-Rei (UFSJ), São João del-Rei-MG, MG, Brazil; Centro Universitário de Sete Lagoas (UNIFEMM), Av. Marechal Castelo Branco, Sete Lagoas, MG, Brazil; Embrapa Milho e Sorgo, Sete Lagoas, MG, Brazil C. G. Sreekala Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Alappuzha, Kerala, India Vishal Tripathi Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, UP, India

Contributors

xiii

Armelle Vallat Neuchatel Platform of Analytical Chemistry, Institute of Chemistry, University of Neuchatel, Neuchatel, Switzerland Camila Cristina Vieira Velloso Universidade Federal de São João Del-Rei (UFSJ), São João del-Rei-MG, MG, Brazil

Part I

Endophytes in Agriculture

Chapter 1

Endophytes in Mineral Nutrient Management: Introduction Dinesh Kumar Maheshwari and Shrivardhan Dheeman

Abstract The second green revolution can beat the challenge of food requirement, which will be a game-changer of this decade. It will boost the fertility of the soil, food security, and global crop production. The microbial world of endophytes having the ability of nutrient mineralization has been proved a boon to mitigate hunger of the global population. In this scenario, crop yields must be increased substantially to glorify the coming decades and mitigate global food demand using endophytesbased biofertilizers. Over the past few years, researchers are engaged to re-discover endophytes to help us to produce healthier crops with higher yields while reducing the need for fertilizer and other chemicals. This is a summary account of reviews of the subject experts from the entire globe bringing their idea(s), commentaries, and views on the current research on endophytes and the mechanistic role of endophytes to sustain agriculture production in major and micro mineral nutrient management precisely. Keywords Endophytes · Mineral nutrients · Soil · Rhizosphere

1.1 Introduction Research of plant growth-promoting bacteria (PGPR) and endophytes is entering in the third decade of the twenty-first century. Scientific chronicles are converting old policies of agriculture into golden policies for sustainable agriculture, to achieve a new revolution and combat against food security. Like plant growth-promoting bacteria, endophytes are also known for providing several direct and indirect benefits to their host friend. Hence, newer studies become important to understand and D. K. Maheshwari · S. Dheeman Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India S. Dheeman (B) Department of Microbiology, School of Life Sciences, Sardar Bhagwan Singh University, Dehradun, Uttarakhand 248 161, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_1

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harness the beneficial influence of the past and future of mineral nutrient management and sustainable agriculture by endophytes. Nutrient management is an approach of sustaining mineral nutrients in plants and soil systems. Originally, this approach is a derivation of integrated nutrient management (INM) holding focus on nitrogen (N), phosphorus (P), and potassium (K) nutrients by blending agrochemicals with effective microorganisms (EM). In the insights of mineral nutrient management (MiNuM), endophytes have been used to increase the spectrum of soil fertility and mineralization or immobilization of various trace elements like N, P, K, Zn, Fe, Cu, Mg, and S. The soil microorganisms can improve plant responses against biotic and abiotic stresses and aid them in health management are called ‘beneficial bacteria’. Altogether the plant-microbe-soil creates a tripartite relationship in soil ecology, which is often studied under plant-microbe interaction. Plant-microbe interaction (PMI) is a complex relationship that exists above-ground and below-ground. The belowground PMI is more complex than the above, because of consisting complex interface with soil. The soil affects these relationships via its physico-chemical properties in addition to abiotic and biotic factors. Few PGPR develops an intimate relationship with plants and becomes colonized inside tissues without any visible symptoms that are usually termed as endophytes. Endophytes are also found in the seeds of few plants, thus, these are termed as ‘seed endophytes’. Basically, in the below-ground PMI, they are known for their versatility and helping plant via several mechanisms such as nitrogen fixation, phosphate solubilization, potassium (K) and zinc (Zn) solubilization, siderophores production, phytohormone production, volatile production of hydrogen cyanic (HCN) acid, 1aminocyclopropane, 1-carboxylic acid (ACC) deaminase production, biocontrol of fungal phytopathogens, induced systemic resistance (ISR) and systemic acquired resistance (SAR). Endophytes are important to consider in the usage of nutrient mineralization due to their significant traits (Maheshwari and Dheeman 2019). The heterogeneous community of endophytes includes root-nodulating Rhizobia to facultative endophytes such as Bacillus, Pseudomonas, Azotobacter, etc. The abundant existence of Bacillus in soil may be attributed due to spore formation, resistance to high temperature, and cold shock resistance (Pandey et al. 2018). Endophytes can solubilize phosphorus (P) and potassium (K) along with the ability to mineralize Zinc (Zn) and oxidize sulfur (S). On the other hand, few endophytes involve in Nfixation (mineralization of N to fix in the form of Ammonia). This way, endophytes have emerged as a versatile candidate. They endure in harsh environments with their feasible strategies and deals with the limitation of agricultural production caused by soil factors. The exact mechanism by which endophytes improve plant health remains largely speculative; however, possible explanation includes mineral nutrient management (include acquisition of nutrients as direct involvement in plant growth promotion largely reviewed in this book by eminent scholars). Endophyte to serve as biofertilizer or Phyto-stimulator helps in maintaining the soil. These include the acquisition of nutrients as a direct involvement in plant growth promotion; however, other mechanisms support indirectly toward plant growth and sustainable agriculture.

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The beneficial microorganisms have been established for efficient mineral solubilization, mobilization, and acquisition of soil nutrients. Being major tissue colonizer of plant’s interior and to improve plant growth by enhancing nutrient use efficiency (NUE) with phosphorus (P) from the organic stock to available form via nutrient mineralization. Biological control against few soil-borne diseases and improved water uptake in drought conditions via the maintenance of ACC-deaminase activity and ethylene regulation influence growth promotion (Aeron et al. 2019). A revised scheme of the utilization of endophyte as bioformulation is depicted in Fig. 1.1. The use of fertilizers, including mineral fertilizers and organic manures, to enhance soil fertility and crop productivity (Etesami and Maheshwari 2018) has often influenced the complex system of the biogeochemical cycles. The synthetic fertilizer and chemicals caused leaching and nutrients run-off, especially N and P, leading to environmental degradation. Low fertilizer use efficiency and continuous long-term use are important causes of this aggravated problem. Thus, it necessitates the involvement of endophytes to acquire suitable strategies for the plant’s mineral nutrient management.

Fig. 1.1 A revised scheme of isolation and characterization of endophytes for plant growth promotion, molecular identification, and use as bioinoculant for raising agricultural crops

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1.2 Frontiers of Endophyte The frontiers of endophyte research have been determined with unique mixes of varied contributions of the chapters and unification of the most influential researches, and historical advances. It finds more about how endophyte owns their frontiers and go beyond.

1.2.1 Avenues in Pharmaceuticals Metabolism is a universal phenomenon of all living creatures and science evidenced the beneficial and harmful gears of metabolites. Most in cases secondary metabolites are considered toxic, and due to antibiosis mechanisms, some sort of bacterial metabolites is considered beneficial for therapeutic purposes. Chapter 6 encased with direct shreds of evidence to understand the usage of secondary metabolites from endophytic fungi. It is focused on biological activity correlated to chemical diversity and exclusive use in agriculture, medicine, and industry.

1.2.2 Fungal Endophytes In the micro-niche of mycorrhizal spore, actinobacterial endophyte creates a scope of future research. As a plant growth promoter, they bear vast applications in agriculture. Actinobacteria lives in association with arbuscular mycorrhizal (AM) spores under abiotic and biotic stresses and, therefore, can alleviate climatic adversity in grain crops like rice; fairly reviewed in Chapter 10. A few endophytic fungi living asymptomatically within the plants can confer improvement in plant nutrient uptake, as a need of a sustainable farming and soilrecharge with biogeochemical cycle. Fungi boost nutrient uptake via several mechanisms understood in Chapter 3. This countered on how fungi hold multiple benefits to plants under stressed conditions and mineral nutrient uptake.

1.2.3 Spore Bearing Endophyte Enhancing Plant Nutrient Uptake Abiotic factors are determinantal for plant growth but, a few endophytes like sporeforming bacilli are resistant to the climatic adversity and contributing to the agricultural productivity. These microorganisms can enhance crop growth with great potential while having an endophytic life. Especially in tropical ecosystems, they colonize the internal tissues of plants and bear an ecological advantage explored

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by their genomics. Thus, opportunities to commercialize these beneficial bacteria, create a deep-down sense to investigating more about their roles and mechanisms has been covered in Chapter 7.

1.2.4 Endophyte for Crop Protection Plant-microbe interactions have many faces of benefit and deleterious effects. In this trend, endophytes diminish disease development by several mechanisms but, precisely by involving antagonistic and parasitic interaction with pathogens. ISR and SAR contributed by endophytes using a sum of different strategies. Hence, endophytes are now utilizing as a source of biological control. Endophyte in biological control and an image that they’re intertwined in the network for mineral nutrient uptake/management.

1.2.5 Phosphorus Management by Endophytes Phosphorus (P) is the second most essential mineral nutrient after nitrogen for plant growth and development. Phosphate solubilizers have been characterized as an important candidate for soil microbes. Like PGPR, endophytic microorganisms associated with different plants release organic acids and solubilize phosphate complexes into ortho-phosphate for easy uptake by plants. Genetic manipulation in the strains of phosphate solubilizing (PS) bacteria can increase the capacity and efficacy of PS biofertilizer for sustainable agriculture, significantly covered in Chapter 3. Along with several mechanisms of PGPR, phosphate solubilization facilitates the conversion of insoluble P and intertwines in the biogeochemical cycle. Chapter 9 reviews the urgency of industrial agriculture to move for modern agricultural biotechnology and exploiting microbial inoculants, which can enhance plant growth and thereby reduce the use of agrochemicals. In this way, giant information on endophyte involved in P solubilization becomes crucial to be collected. This chapter focused on endophytic phosphate solubilization and its role in mineral management.

1.2.6 Endophytes: Ecological Advances The realization that the plant microbiome can improve the management of plant health, soil fertility, and crop productivity is one of the most fascinating scientific discoveries in the world. Endophytic bacteria are unique plant microbiome that establishes them within their tissues. Chapter 12 is enhancing wisdom on putative functions of endophyte for plant mineral nutrients acquisition and is advantageous to provide better opportunities and viable strategies for sustainable agriculture.

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1.2.7 PGPB: Nutrient Use Efficiency Plant growth-promoting bacteria (PGPB) has a potential tool for sustainable agriculture utilizing for a long time in plant growth and development. Also, these PGPB increase plant nutrient uptake capacity and nutrient use efficiency. Chapter 13 illustrates several studies focusing on PGPRs in nutrient use efficiency of various crops and covered their long-term application to reduce the use, cope with the negative effects of chemical fertilizer thereby.

1.2.8 Iron Management: Endophytes in Siderophore Production Iron is an essential nutrient for plant growth and soil salinity is a leading cause for iron limitation. Plants and microbes overcome this iron limitation by producing ironchelating agents known as Siderophores. Effect of Iron on siderophore production, pH levels, antagonism, and root colonization was identified. Chapter 5 is providing a case study for salinity stress by managing iron via siderophore by Pseudomonads being the most dominant bacteria in the soil ecosystem after bacilli. This further strengthens how siderophore is important for soil nutrient management and sustainable farming. In the plant-soil interaction uptake of nutrients specifically, phosphorus, nitrogen, iron, and potassium is facilitated by plant growth-promoting rhizobacteria. Recently, endophyte was identified to produce a variety of siderophores such as pyoverdine, hydroxymate, ferrioxamines increase three times iron transportation efficiency to the plant for the development of root and shoot growth. Chapter 14 understands the applications of siderophore in bioremediation, weathering of soil-mineral particles, and plant growth as a major account.

1.2.9 Endophyte: Biotechnology and Bioinformatics Endophytes have emerged as an important tool for plant growth promotion and crop productivity enhancement. Their application is extending the frontiers of medicine industry and environmental remediation. Chapter 8 is an important part of elaborating major findings of endophytes and their applications in emerging ‘omic’ tools and to cast the light on biotechnological and bioinformatics aspects.

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1.3 Conclusions In current scenario, due to the abundant use of synthetic chemicals on crops, the sustainability of agriculture systems has distorted; the cost of cultivation has increased at a high rate; the income of farmers stagnated, and the provision of food security and safety has become a frightening challenge. For these reasons, estimation and re-investigation of the endeavors of endophytes via mineral nutrient mineralization become important. The harmless inputs in safeguarding soil health and the quality of crop products are holding the inspiration to scientists to re-discover multi-faceted roles of endophytes in plant interaction and benefits to agriculture. The use of endophytes is a relevant strategy for the efficient and rational use of agricultural resources with minimal effects of adverse environmental impacts that may boost water resources, ecosystems, or the quality of human life.

References Aeron A, Khare E, Jha CK, Meena VS, Aziz SM, Islam MT, Kim K, Meena SK, Pattanayak A, Rajashekara H, Dubey RC (2019) Revisiting the plant growth-promoting rhizobacteria: lessons from the past and objectives for the future. Arch Microbiol 28:1–2 Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Safe 156:225–246 Maheshwari DK, Dheeman S (2019) Field crops: sustainable management of PGPR. Springer, Switzerland, p 458 Pandey C, Bajpai VK, Negi YK, Rather IA, Maheshwari DK (2018) Effect of plant growthpromoting Bacillus spp. on nutritional properties of Amaranthus hypochondriacus grains. Saudi J Biol Sci 25(6):1066–1071

Chapter 2

Bioefficacy of Endophytes in the Control of Plant Diseases Fernando Matias Romero, Amira Susana Nieva, Oscar Adolfo Ruiz, Andrés Gárriz, and Franco Rubén Rossi

Abstract Plants establish multiple kinds of interactions with microorganisms, which can be neutral, beneficial, or detrimental for the plant host. Interactions also occur between endophytic microorganisms that colonize inner parts of plants, beneficial in nature, and able to promote plant growth both directly or indirectly. Direct plant-growth promotion includes the production of phytohormones, nitrogen fixation, and an increase in nutrient availability. On the other hand, endophytes can promote plant growth indirectly by contributing some beneficial attributes to plant health. Direct interaction between pathogens and endophytes also induces systemic resistance in the host, which allows the plant to respond faster and/or more intensively upon pathogen infection. Usually, endophytes share more than one of these mechanisms so the outcome of the interaction is the sum of different strategies. In this chapter, review on bacterial and fungal endophytes as potential biological control agents and their mechanisms of action have been documented. Besides it analyzes the most recent information about the nutrient uptake/management, specifically iron and nitrogen nutrition, with the biological control exerted by beneficial microorganisms. Keywords Endophytes · Biological control · Plant protection · Biological control agents

2.1 Introduction Control of plant diseases that reduce crop yields is a pressing need in modern agriculture, as the demands of stable and healthy food supplies by a growing human population must be guaranteed (Emmert and Handelsman 1999; Maheshwari 2013; Maheshwari and Annapurna 2017). Although there are several strategies to control plant diseases, there is an increasing interest in finding new technologies that can F. M. Romero (B) · A. S. Nieva · O. A. Ruiz · A. Gárriz · F. R. Rossi Instituto Tecnológico Chascomús, Universidad Nacional de General San Martin-Consejo Nacional de Investigaciones Científicas y Técnicas (INTECH/UNSAM-CONICET), Chascomús, Argentina e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_2

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diminish or replace the use of agrochemicals, which can result in negative consequences to human health and the environment. In this way, biological control has attracted the interest of researchers over the last few years as a non-polluting alternative. One of the many strategies is to adopt microbial inoculants since they have several benefits compared to traditional chemical pest management. Being effective in small quantities, because they can multiply themselves, and at the same time, the host and the native microbial community control their spread (Berg 2009). Another advantage of bioinoculants is that the development of resistance is limited because of the involvement of different control mechanisms simultaneously. Moreover, microbial inoculants can be used in conventional or integrated pest management (Berg 2009). Thus, it can be achieved by (i) creation of environmental conditions favorable for the action of controlling microorganisms already present in the crops, (ii) through the genetic improvement of the host’s ability to interact with such microorganisms and (iii) by the genetic manipulation of the controlling microorganisms to give them advantageous characteristics, or the massive introduction of beneficial microorganisms into the host during the interaction process. The first microorganisms receiving attention as potential bioinoculants were those inhabiting the host-rhizosphere because they were proven to have several traits regarding plant promotion and antagonistic activity against plant pathogens (Bhattacharyya and Jha 2012). However, the microorganisms able to colonize the inner cells and tissues of plant hosts also improve plant growth and health and seem to be excellent candidates as biological control agents (BCAs) as observed by several workers (Berg and Hallmann 2006; Kloepper and Ryu 2006; Maheshwari 2017). It is due to endophytic nature which is better protected from harsh environmental conditions (i.e. extreme temperatures and UV light) and is in closer contact with their host’s cells and tissues than that of rhizosphere or phyllosphere microbes (Hallmann et al. 1997; Lindow and Brandl 2003). A great diversity of microorganisms were reported to exist as endophytes in cultivation-based studies (Reinhold-Hurek and Hurek 2011; Suryanarayanan 2013). Among the bacterial endophytes, most isolates belong to the phylum Proteobacteria, even though Firmicutes, Actinobacteria, and Bacteroidetes were also represented (Rosenblueth and Martinez-Romero 2006). However, diversity and richness of endophytic communities are much greater than those reported in culture-dependent studies (Dissanayake et al. 2018). In this trend, the use of next-generation sequencing (NGS) techniques has helped to unravel the structure and composition of endophytic communities more truly (Bulgarelli et al. 2012; Hong et al. 2019; Romero et al. 2014). The rapid development and the relative low costs of NGS have contributed to study microbial communities associated to different plant genotypes and/or growth stages (Manter et al. 2010; Marques et al. 2014) and is helping to get new insights into dynamics of plant-endophyte-pathogen interactions (Ardanov et al. 2012; Bulgari et al. 2014; Tian et al. 2019). Moreover, these culture-independent technologies not only exhibit the composition of the endophytic communities but also, facilitate the study of the functions performed by communities in the system. However, the analysis of biological control (BC) related traits in endophyte microbial communities is

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still scarce. This information could lead to the development of improved and more efficient BCAs for sustainable agriculture. In this chapter, we will review and summarize some of the works reporting the use of microbial endophytes as biological control agents for different plant diseases and their mechanisms of action. Finally, we will discuss the nutrient uptake/management during biological control mediated by beneficial microorganisms.

2.2 Bacterial Endophytes as BCAs Endophytic microorganisms can display one or more mechanisms of action toward a specific pest or pathogen including direct interactions between endophytes, pathogens, and their hosts and this is one of the reasons why the use of microbial inoculants has notable advantages against chemical treatments (Fig. 2.1). The most commonly described mechanisms include inhibition of the pathogen by the

Fig. 2.1 Modes of action in plant-microbe interactions promoting plant growth and health

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production of antimicrobial compounds, competition for nutrients and space, induction of plant defense mechanisms, and parasitism. However, other modes of action remain to be explored in-depth, as the inactivation of pathogen germination factors or even degradation of virulence factors such as toxins produced by phytopathogens (Whipps 2001). Further, endophytes possess significant efficiency of protection since it is possible to prepare bioformulations with more than one microorganism for multiple trait benefits to combine desired traits and/or efficacy (Aeron et al. 2011; Baliyan et al. 2018; Pandey and Maheshwari 2007). For instance, Varo et al. (2016) tested several BCAs alone or in combinations, which showed great levels of protection against wilt in olives caused by Verticillium dahlia, reducing the incidence and mortality up to 90% (Varo et al. 2016).

2.2.1 Antagonism Since endophytes share a similar niche as of many phytopathogens colonizing plant cells and tissues, with different degrees of association direct antagonism between them is a reliable screening technique to screen potential BCAs from a collection of endophytic isolates. Microbial balance in the tissue of plant, as a micro-niche microbial homeostasis is also important to notice, where microbe-microbe interactions interplay. The native microbe of endophytic nature sometimes competes with the other invading microbe under natural conditions. The in vitro proves of this phenomenon are constant and yet few. Direct inhibition of pathogens is mainly mediated by the synthesis of antibiotics, volatile production of hydrogen cyanide (HCN), and antifungal metabolites (Raaijmakers et al. 2002, 2010). Antibiotics encompass a chemically heterogeneous group of organic, low-molecular-weight compounds. At low concentrations, these are deleterious to the growth or metabolic activities of other microorganisms, and most BCAs bacteria produce multiple antibiotics with different degrees of efficacy against pathogens, some of them with overlapping activity. Several compounds have been purified and identified from biocontrol bacteria. For example, pyrrolnitrin is produced by bacteria from the genus Pseudomonas and Burkholderia, which has been proven to be effective against a wide variety of plant pathogens such as Rhizoctonia solani, Botrytis cinerea, V. dahliae, and Sclerotinia sclerotiorum (Raaijmakers et al. 2002). Moreover, mutant strains unable to produce this compound lost the in vitro and in planta ability to control R. solani (Hill et al. 1994). In turn, 2,4diacetylphloroglucinol (DAPG) is a phenolic antibiotic produced by BCAs from the genus Pseudomonas that exhibits antibacterial, antifungal, and anthelminthic activity (Haas and Defago 2005; Weller et al. 2007). DAPG not only was proven to inhibit the growth of pathogens directly but also, it has been demonstrated that Arabidopsis thaliana inoculated with Pseudomonas sp. mutant strains unable to produce DAPG are impaired in developing induced systemic resistance (ISR) against Pseudomonas syringae pv. tomato (Weller et al. 2012). Phenazines are also a class of well-studied natural antibiotics that are produced by diverse plant-associated bacteria, exhibiting

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unique redox properties and broad-spectrum antibiotic activity, and playing a wide variety of roles in nature (Mavrodi et al. 2006). Endophytes are essential to the production of several secondary metabolites in grasses, in the process of gummosis in trees, and the production of useful metabolites such as alkaloids, pestaloside, cryptocandin, enfumafungin, subglutinols, etc., for the host plant (Maheshwari and Annapurna 2017). The transformation of P. fluorescens strain Q8r1-96 with the biosynthetic locus leading to the production of phenazine-1-carboxylic acid, a precursor of several phenazine compounds, conduces to an increase in the biocontrol efficacy against Rhizoctonia root rot in wheat. In this trend, a lower dose of the transformant antagonist is required to exert the similar level of control exerted by the parental strain (Huang et al. 2004). The presence of these traits in soils is thought to explain disease decline in suppressive soils, in which specific soil-borne plant pathogens cause only limited disease although the pathogen and susceptible host plants are both present. However, the quantification of these characteristics in different types of soils has no clear correlation between the presence of antibiotic synthetic genes and disease suppression (Garbeva et al. 2004; Imperiali et al. 2017). Further analysis is required to understand how these are expressed genetically and regulated in soil and/or inside plants. Other metabolites with direct action against bacteria and fungi are lipopeptides such as iturin, surfactin, thanamycin, and fengycin (Ongena and Jacques 2008; Raaijmakers et al. 2010); and also the polyketide antibiotics bacillaene, difficidin, and macrolactin produced mainly, but not exclusively, by different strains of the genus Bacillus. The role of these compounds in biocontrol activity was also evidenced by the use of mutant strains defective in their production. For instance, the biocontrol activity of B. subtilis strain 6051 against P. syringae in Arabidopsis was impaired when a mutant strain unable to produce surfactin was used (Bais et al. 2004). Similarly, Pseudomonas strain SH-C52 reduces the incidence of stem rot disease of groundnut, whereas a thanamycin-deficient mutant strain was less effective (Le et al. 2012). Non-ribosomal peptides also contribute to the antagonism against bacteria and fungi (Abdalla and Matasyoh 2014). For instance, Tontou et al. (2015) demonstrated that an endophytic strain of P. synxantha isolated from Actinidia chinense showed antagonism against P. syringae pv. actinidiae (Psa) in vitro. To find out the molecular mechanisms involved in the antagonism, a mini transposon-mutant library was constructed and antagonism-deficient mutants were selected. Molecular characterization of these mutants showed that three genes could be involved in antagonistic activity, an acyl-homoserine lactone acylase gene, a glucose-6-phosphate dehydrogenase gene, and an mbtH-like gene. As these genes are directly or indirectly involved in the synthesis of non-ribosomal peptides, the authors claimed that these molecules are involved in the antagonistic ability of P. synxantha (Tontou et al. 2015). However, it is worthy to mention that these genes could also be affecting other antagonismassociated mechanisms. Thus, it has been shown that quorum sensing perturbation by the action of acyl-homoserine lactone degrading enzymes can interfere with interspecies competition (Amara et al. 2011; Kusari et al. 2014).

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Even though the identity of the antimicrobial molecules has not been determined so far, several other studies proved that endophytic bacteria produce compounds with antimicrobial activity. These studies typically used cell-free supernatants from the cultures of these isolates and to inhibit the in vitro growth of phytopathogens. For instance, bacterial endophytes identified as Pseudomonas, Bacillus, and Pantoea isolated from field-grown tomato leaves showed antagonism against bacterial (P. syringae) and fungal (Botrytis cinerea) pathogens in vitro and planta (Romero et al. 2016). Moreover, their cell-free supernatants were able to inhibit the germination of conidia from B. cinerea for about 30–60% and also stopped the growth of P. syringae when added to growth media. Additional pieces of evidence of antibiotic production were demonstrated using a semi-purified ethyl acetate extract of the endophyte B. velezensis EB-39 against Xanthomonas campestris subsp. citri (Rabbee et al. 2019). Interestingly, this extract showed similar inhibitory activity to that observed in confrontation assays between EB-39 and X. campestris. Purification and identification of new compounds from new isolates will increase the possibility to develop new biocontrol strategies using whole microbes or their cell free metabolites alone. The presence of genes involved in the biosynthesis of different antimicrobial compounds was also used as an indication of the ability to produce this kind of metabolites. An analysis performed on cultivable bacterial endophytes from mulberry cultivars having different resistance to sclerotiniosis showed that endophytic communities from resistant genotypes are more diverse than those from the sensible ones (Xu et al. 2019). In this work, dual-culture assays were performed with these endophytes against S. sclerotiorum, B. cinerea, and Colletotrichum gloeosporioide and most of the isolates that inhibit fungal growth were positive for the presence of genes involved in the biosynthesis of antimicrobial compounds, such as polyketides, non-ribosomal peptides, surfactin, iturin, and fengycin (Xu et al. 2019). Following this approach, Cui et al. (2019) isolated a B. amyloliquefaciens strain from Chinese cabbage with antagonistic activity against Pectobacterium carotovorum subsp. carotovorum, the causal agent of soft rot, possess genes involved in polyketides and dipeptide biosynthesis and showed a level of protection up to 75% in greenhouse experiments (Cui et al. 2019). It is worthy to mention that the mere presence of these biosynthetic genes is not sufficient to confirm the production of the antimicrobial molecules. For instance, Hazarika et al. (2019) demonstrated that a B. subtilis strain isolated from sugarcane as well as cell-free supernatants obtained from its culture showed antagonism against several pathogens. Moreover, it was positive for the presence of different genes involved in the synthesis of antimicrobial compounds, even though only one of them was detected in supernatants (surfactin) (Hazarika et al. 2019). This observation indicates that gene expression in combination with gene presence would be a more accurate indicator of antagonistic potential. Volatile organic compounds (VOCs) are also responsible for the ability of certain isolates to inhibit the in vitro growth of different pathogens. For instance, an endophytic isolate from black pepper roots identified as P. putida inhibits the growth of several plant pathogens due to the production of volatile compounds as revealed by Gas Chromatography/Mass Spectrometry (GC/MS) (Sheoran et al. 2015). Moreover, the application of some of these chemically synthesized VOCs showed a high

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percentage of protection on black pepper shoots against Phytophthora capsici, especially when these compounds were applied at low concentrations (Agisha et al. 2019). The production of VOCs was also evidenced and identified in two isolates from cocoa that showed antagonism against the causal agent of a black pod, Phytophthora palmivora, both in vitro and in planta (Alsultan et al. 2019). The role of VOCs in plant protection is not only due to the direct effect on pathogen’s growth as there is evidence that 2,3-butanediol and acetoin can induce systemic resistance to pathogens (Ryu et al. 2004).

2.2.2 Induction Disease Resistance in Plants The recognition of microbial cell components and/or their metabolites can induce in the host’s physiological state allowing them to respond faster and/or to a greater extent to future pathogenic attacks. This phenomenon is called induced systemic resistance (ISR) and shares characteristics with another type of systemic resistance triggered by a previous attack of the necrosis-producing pathogen (SAR, systemic acquired resistance). There are two possible molecular mechanisms activated during ISR. Thus, endophyte-inoculation can induce the expression of defense-related genes per se, or on the other hand, the presence of beneficial microorganisms primes plants for enhanced defense responses. In primed plants, defense responses are not activated directly but are potentiated upon pathogen attack, resulting in enhanced resistance (van Wees et al. 2008). Both ISR and SAR contribute to resistance to a wide range of pathogens in systemic host´s tissues. However, the molecular mechanisms underlying both processes may differ. It was initially proposed that ISR is independent of salicylic acid (SA) signaling pathways but dependant of jasmonic acid (JA) and ethylene (ET), while SAR is dependant of SA and variable dependant of JA and ethylene (van Loon et al. 1998). However, a great number of systems studied afterward demonstrated that beneficial microorganisms induce resistance by activating both SA- and JA-signaling pathways (Mathys et al. 2012; Niu et al. 2011, 2012) or the SA-signaling pathway alone (Tjamos et al. 2005; van de Mortel et al. 2012). Thus, it is probable that nature and the molecular mechanisms underlying ISR depends on particular combinations of plant-beneficial microorganism-pathogen. Regarding endophyte-ISR induction, it would be strictly necessary to test that endophyte and pathogen are physically separated in the plant to ensure that the mechanism involved in protection is ISR (Kloepper and Ryu 2006). This is difficult to perform with microbial endophytes that colonize the entire plant. In this section, we will discuss some examples of bacterial endophytes inducing defense responses in their host independently of their colonization pattern. Changes in gene expression due to endophyte inoculation can be both local (at the site of inoculation) and systematic (in inoculated and not inoculated tissues). A clear example of systematic responses is the interaction between olives and the endophytic bacterium P. fluorescens PICF7, which conduce to the overexpression of defense-related genes in both roots and

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leaves (Gómez-Lama Cabanás et al. 2014; Schilirò et al. 2012). Another example of induced resistance was described by Sahu et al. (2019), where three Bacillus strains from a collection of endophytes from tomato plants were selected due to their antagonism to Sclerotium rolfsii. These isolates reduced disease incidence up to 67% under greenhouse conditions (Sahu et al. 2019). Moreover, endophyte-inoculation reduced the reactive oxygen species (ROS) generated at the site of the S. rolfsii infection and induced the expression of pathogenesis-related (P R) genes. In this trend, one of the isolates was able to induce the expression of genes PR1a, PR2b, and PR3 in absence of the pathogen, while others showed a mild induction of these genes that was enhanced upon infection with the pathogen. Further, these isolates were able to induce the activity of defense-related enzymes such as phenylalanine ammonia-lyase (PAL), peroxidase, polyphenol oxidase, and ascorbic acid oxidase (Sahu et al. 2019). Importantly, besides their roles in the synthesis of bioactive molecules, these enzymes are involved in plant cell wall reinforcement. Thus, it is probable that their activities can help to prevent the infection by necrotrophic pathogens. This might explain also the mechanism of protection exerted by two Stenotrophomonas strains with the ability to colonize Arabidopsis leaves, which modified the expression of different enzymes involved in cell wall synthesis and reduce lesion sizes provoked by the necrotrophic pathogens S. sclerotiorum and B. cinerea (Marina et al. 2019). Accordingly, when cell wall extracts obtained from inoculated leaves were used as a substrate for pathogens growth on agar plates, there was a reduction in fungal colony radius compared to plates supplemented with cell wall extracts from mockinoculated leaves. Besides, Stenotrophomonas inoculation induced callose deposition and expression of PR genes associated with the SA and JA signaling pathways. Similarly, endophytes isolated from Solanum tuberosum able to induce resistance to Pectobacterium atrosepticum in potato and are able to increase defense-related enzyme activities both before and after pathogen challenge. Moreover, these isolates primed the expression of PR genes involved in both, the SA and JA signaling pathways (Ardanov et al. 2011). The ability to induce the expression of genes involved in phytohormones signaling was also reported by an apoplast-colonizing endophyte from canola leaves (Romero et al. 2019). This isolate showed antagonism against different phytopathogens in vitro and planta. The mechanisms proposed to be involved include the production of antimicrobial compounds as well as the ability to induce defense mechanisms mediated by SA and JA in the host. Transcriptional changes induced by beneficial microbes usually differ from the changes induced by pathogens, mainly in the intensity of induction (Romero et al. 2017). Burkholderia phytofirmans PsJN induced the expression of defense-related genes in grapevine cell suspension but to a lesser extent than non-host bacterium P. syringae pv. pisi. Both bacteria-induced medium alkalization, but the endophyte did not provoke ROS production or cell death, which are observed in pathogentreated cells (Bordiec et al. 2011). This isolate also primed the expression of PR genes involved in the SA and JA signaling pathways upon pathogen infection in Arabidopsis, showing more sustained expression of PDF1.2, a JA dependent PR gene (Su et al. 2017).

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Several plants possess different compounds with antimicrobial activity; this is the case of Allium sativum (garlic) that produces alliin, an alkyl cysteine sulphoxide that is converted to allicin by the enzyme alliinase. Wang et al. (2019) isolated endophytes from garlic and selected two strains showing antagonism against Sclerotium cepivorum, the causal agent of white rot disease. Also, these isolates reduced the disease index by up to 66% in greenhouse assays. The authors proposed that there is not only a direct antagonistic effect due to the production of extracellular enzymes, but also an induction in the production of antimicrobial products in the host. Thus, inoculation with one of the isolates primed the expression of alliinase and the accumulation of alliin (Wang et al. 2019).

2.2.3 Parasitism This kind of interaction is more commonly observed in bacteria-fungi and fungi-fungi interactions. During these interactions, fungal cells are lysed due to breaking down to mycelial cell wall. These effects are due to the action of extracellular enzymes such as glucanases, chitinases, and proteases as well as antifungal compounds (Chauhan et al. 2016; Whipps 2001). For instance, poplar canker provoked by Cytospora chrysosperma, Phomopsis macrospora, and Fusicoccum aesculi can be controlled with an efficiency up to 90% by bacterial endophytes with antagonistic activity against these pathogens due to production of extracellular enzymes such as β-1,3glucanases, proteases, and chitinases (Ren et al. 2011). The important role of βglucanases was evidenced recently in the interaction between B. halotolerans, a cotton endophytic strain, and the pathogen V. dahliae. This endophyte was selected because of the ability to inhibit conidial germination and mycelial growth of the pathogen in vitro and showed β-glucanase activity. Mutant and overexpressing strains were generated to elucidate the role of β-glucanase. In vitro antagonism assays using the mutant strain exhibited diminished antifungal activity against V. dahliae compared to wild type or the complementary strain. In turn, bioassays using the overexpressing strain showed a greater protective effect compared to wild type, as the disease indexes diminished from 17.86 (wild type strain) to 8.33 (overexpressing strain) after 45 days post-inoculation (Zhang et al. 2019a). As mentioned earlier, the protective effects observed by endophyte inoculation usually involved more than one mechanism. For instance, an Enterobacter strain isolated from finger millet roots, has been found as an endophyte in other crops such as maize and wheat showed antagonism against Fusarium graminearum among other pathogens, and it was able to reduce disease symptoms up to 90% in greenhouse trials (Mousa et al. 2016). Interestingly, during confrontation assays, Enterobacter sp. seemed to be attracted to fungal cells, formed biofilms over fungal hyphae, and finally destroy fungal cells. Moreover, when inoculated on roots, the isolates showed the ability to induce proliferation of root hairs and establish a physicochemical barrier to trap and degrade the pathogen hyphae. Biocontrol and antagonistic ability of these endophytes require the production of phenazine, c-di-GMP-dependent signaling

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pathway, and resistance to a Fusarium-derived antibiotic. This was evidenced due to the construction of a Tn5-mutant library, selecting mutant strains that have lost the ability to inhibit the growth of F. graminearum. We here described just some examples of bacterial endophytes with different mechanisms of action, but there is a consistent reporting on the isolation of new endophytic strains from diverse genera of plants to inhibit different phytopathogens. Most of them demonstrated significant effects as BCAs with high levels of protection in planta (Asghari et al. 2019; Etesami and Alikhani 2016; Ferrigo et al. 2017; Ghazalibiglar et al. 2016; Zhang et al. 2019b). Although the exact mechanism of biocontrol exerted by these endophytes has not fully explored so far, these constitute a valorous collection of microorganisms for the development of biotechnological applications (Maheshwari and Annapurna 2017).

2.3 Fungal Endophytes The term “endophyte” is applied to fungi which has been redefined according to the permanence of the microorganism inside host tissues, the symptomless character of the infection, and the benefits provided by the fungi to the plant host. This is because, over the years, research regarding fungal endophytes has incorporated functional information besides infection traits. In this trend, several functions such as defensive mutualism, nutritional uptake, and the production of secondary metabolites improving plant fitness have been considered (Rodriguez et al. 2009; Schulz et al. 2002). Hyde and Soytong (2008) analyzed several definitions of fungal endophytes taking into account different traits, from infection and symptom development to ecological functions. This changed the study of fungal endophytes into new perspectives taking into consideration the permanence of mutualism, stability of the interaction, and evolutionary features. Fungal endophytes belong to a group with great taxonomic diversity (Arnold et al. 2000, 2001; Rodriguez et al. 2009), which are classified according to their identity and functional roles. Thus, fungal endophytes were divided into two groups: Clavicipitaceous and Non-Clavicipitaceous (Rodriguez et al. 2009). Nevertheless, it has been exhibited that most fungal endophytes studied to date corresponds to the phylum Ascomycetes (Lugtenberg et al. 2016).

2.3.1 Clavicipitaceous Fungal Endophytes (Grass-Endophytes Interactions) Epichlöe-temperate grasses are the most studied models included in this category (Omacini et al. 2012). The interactions between grasses and endophytes are clustered in Group I, belonging to the Clavicipitaceae family in correspondence with the

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classification proposed by Rodriguez et al. (2009). In these interactions, fungi inside plant tissues can produce ergot alkaloids that prevent against parasitoid infections, mainly represented by herbivores insects (Bacon et al. 1986; Torres et al. 2008). These plant-fungal interactions affect directly the insect abundance with consequences in the balance of the food-web dynamics (Omacini et al. 2001). Also, a recent study has demonstrated another protective mechanism involved in Epichlöe-grass systems that are based on the alteration of the plant odor to attract aphid predators (Fuchs and Krauss 2019). Endophytes-grass interactions have been described as mutualism. In this sense, Clay (1988) has described endophyte-grass interactions as a “defensive mutualism.” Further studies have demonstrated that the effects of these interactions depend on global factors, such as plant genotype and environmental conditions, leading to neutral situations or turning into a pathogenic outcome (Faeth and Fagan 2002; Müller and Krauss 2005; Saikkonen et al. 2006). The research conducted on endophyte-grass interactions is oriented to a better understanding of the effects on all the components of the ecosystem. For example, it has been studied the relation between grass-endophytes, growth and fecundity of their hosts, and the further reconstruction of the plant community with the implication in the restoration of prairies (Moore et al. 2019). On the other hand, some studies analyzed the effect of endophytes on other soil microorganisms such as mycorrhizal fungi (Kalosa-Kenyon et al. 2018), and the cattle in agro-ecosystems (Bultman et al. 2018). Since transmission of grass-endophytes occurs horizontally as well as vertically, it protects all the plant tissues in every plant generation (Rodriguez et al. 2009). This phenomenon would help the establishment of certain plant species in particular environments, which denotes the evolutionary impact of this kind of interaction, in which the permanence of plant species may be a consequence of the interaction with particular fungal endophytes (Saikkonen et al. 2004). Thus, grassland protection conferred by endophytes makes these microbes beneficial for augmenting integrated pest management programs and considering sustainable agriculture premises (Kauppinen et al. 2016).

2.3.2 Non-Clavicipitaceous Fungal Endophytes Despite most research on fungal endophytes is represented by the grass-endophytes interactions, there is increasing interest in fungal endophytes belonging to the NonClavicipitaceous group, as these fungal endophytes are also able to impair the proliferation of pathogens and decrease the severity of symptoms by direct interaction (Arnold et al. 2000). Interestingly, fungal endophytes can reduce pathogenic infections even when both organisms are closely related. For example, Colletotrichum magna can infect Cucumis sativus and confer protection against C. orbiculare and F. oxysporum (Redman et al. 1999). This evidence demonstrates that despite the pathogenic role of certain fungi, such as Fusarium species, they are also able to

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perform endophytic interactions and even promote plant growth as evidenced by Nieva et al. (2019) who demonstrates growth promotion effects by F. solani in the model legume Lotus japonicus (Nieva et al. 2019). Root fungal endophytes play an important role in plant growth due to involvement in nutrient and water acquisition (Lugtenberg et al. 2016). Dark septate endophytes (DSE) constitute a group of fungal endophytes characterized by their ability to colonize roots without causing damage and having melanin in their hyphae. They have been defined as multifunctional, taking part in different processes such as nutritional uptake improvement, abiotic stress tolerance, and heavy metal sequestration (Mandyam and Jumpponen 2005). Besides, they might play important roles as BCAs. In this trend, there is evidence of DSE fungi controlling V. dahliae in tomato, showing a reduction of up to 30% in disease symptoms (Andrade-Linares et al. 2011). Another example is the endophytic fungus Phialocephala fortinii, exhibited75% of inhibition against F. oxysporum in Asparagus officinalis (Narisawa 2018). Besides, in vitro antagonism between DSE, ectomycorrhizal fungi, and pathogens such as Pythium intermedium, Phytophthora citricola, and Heterobasidion annosum has been evaluated (Berthelot et al. 2019). These results could help the development of fungal consortia to be used as phytostimulant and/or biocontrol products. Fungi belonging to the Trichoderma genus have been demonstrated to be important biocontrol agents as they manage to induce ISR by activating the JA and SA signaling pathways (Mukherjee et al. 2012). To date, this organism is the most important bio-fungicide developed and commercialized around the world (Verma et al. 2007), where the use of different Trichoderma spp. strains in disease biocontrol have been extended to several crops and landscapes. Moreover, colonization of maize plants by T. atroviride also induces resistance against herbivores such as Spodoptera frugiperda (Contreras-Cornejo et al. 2018). In turn, yeast endophytes have been scarcely studied to date. There are evidence that these organisms survive as endophytes in Z. mays (Nassar et al. 2005) and in stomata and xylem vessels of Citrus sinensis (Gai et al. 2009), but their potential as biocontrol agents is yet to be evaluated. Recently, Rhodotorula and Cryptococcus sp. have been proposed as biocontrol agents against the “witches’ broom disease” of cacao (Ferraz et al. 2019).

2.3.3 Mechanisms of Biological Control by Fungal Endophytes Biological control mediated by fungal endophytes involves the production of secondary metabolites, such as alkaloids, antibiotics, and/or lytic enzymes (Gao et al. 2010). Also, as mentioned earlier for bacterial BCAs, volatile compounds produced by fungal endophytes have been proposed as good biological control agents (Morath et al. 2012). For example, volatile metabolites produced by the endophyte

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F. oxysporum CanR-46 control the impact of S. sclerotiorum in Brassica napus, demonstrating a 94.5% mycelial growth inhibition (Zhang et al. 2014). Moreover, fungal endophytes have been proposed as sources of useful secondary metabolites (Petrini et al. 1993; Schulz et al. 2002; Shukla et al. 2014). In this trend, there is an interesting research field focused on the bioactive compounds produced by endophytic fungi and their applications in agriculture, medicine, and industry (Zhao et al. 2011). The use of endophytes to promote plant fitness could improve the production of medicinal plants as well as their bioactive-derivate compounds in medicinal plants (Jia et al. 2016). Besides parasitism and antibiosis, Trichoderma spp. can manage to induce lipid transferase proteins to confer defense against Phytophthora capsici (Bae et al. 2011). Induction of systemic resistance was also evidenced by the activation of defenserelated enzymes on cucumber plants inoculated with a non-pathogenic strain of Colletotrichum magna (Redman et al. 1999). Timing is an important factor to ensure a successful biocontrol strategy. In this trend, the order of arrival of endophytes and pathogens in Phaseolus lunatus was analyzed (Adame-Álvarez et al. 2014). Interestingly, the antagonist effect of the endophytes on the pathogen was only successful when the endophyte colonization occurs first; otherwise, endophyte inoculation after pathogen infection rather facilitates disease development (Adame-Álvarez et al. 2014). As mentioned earlier, fungal endophytes can trigger ISR in the host. The mechanisms involved in this response are analogous to those imposed by mycorrhizal fungi, involving the SA and JA signaling pathways (Jung et al. 2012; Pozo and AzcónAguilar 2007). In a previous study, it has been demonstrated that JA is necessary for the biocontrol response in tomato triggered by the infection of a non-pathogenic F. solani strain (Kavroulakis et al. 2007). In this system, F. solani can elicit ISR against Septoria lycopersici by expression of pathogenesis-related (PR) genes in roots. In agreement with the effects reported for bacterial endophytes, it has been demonstrated that ethylene, as well as JA, is required for ISR triggered by fungal endophytes (Kavroulakis et al. 2007). Nevertheless, a recent study has demonstrated that inoculation with an endophytic Fusarium strain can trigger the systemic response independently of JA, SA, and ethylene (Constantin et al. 2019). As exposed above, the interactions between grasses and fungi belonging to the Clavicipitaceous group constitute protective mutualisms. The effect of the endophyte-infected grasses (E+) on the dynamic population of the insect pest has been extensively compared with the non-endophyte infected grasses (E−). For example, Lolium multiflorum-E. occultans interaction reduces the aphid population by 64% and the nymph by 81%, consequently, the fecundity of the aphid populations is strongly affected (Bastias et al. 2017b). Complementary to the protection conferred by the alkaloids production, recent studies on the endophyte-grass interactions has demonstrated the ability of the endophyte to enhance the plant immunity through mechanisms involving the JA-mediated response, by the promotion of JA-signaling and repression of SA-signaling defenses (Bastias et al. 2017a). Besides, the interaction between Lolium pernenne-Epichlöe

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festucae var lolii system displays the differential expression of 38% of the genes expressed between E+ and E− plants (Dupont et al. 2015). The property of some entomopathogenic fungi to control insect pests, and at the same time survive as endophytes, may also improve ISR and confer dual protection (Jaber and Ownley 2018). In this trend, it might be possible that biological control transcends the plant-microorganism system which can be extrapolated to other components of the ecosystem.

2.4 The Relation Between Nutrient Management and Biological Control Besides the roles played by endophytes in biological control described in this chapter, many pieces of evidence show that they are also involved in mineral nutrition. This is important since the facilitation of nutrient uptake by their hosts contributes to plantgrowth promotion (Maheshwari and Annapurna 2017). Even though there is little information regarding the relation of nutrient uptake/management with biological control traits displayed by beneficial microorganisms, there is evidence of crosstalk between iron starvation responses and ISR triggered by beneficial rhizobacteria. The comparison of the genes induced by Pseudomonas spp. WCS417 with the iron-deficiency root transcriptome showed that 20% of the regulated genes are activated in both conditions (Zamioudis et al. 2015). One of these genes is the rootspecific R2R3-type MYB transcription factor MYB72, that was described as a key component of ISR triggered by beneficial microbes (Segarra et al. 2009; Van der Ent et al. 2008) as well as an important player in the iron deficiency response (Buckhout et al. 2009; Colangelo and Guerinot 2004). Interestingly, a deeper insight into the molecular mechanisms involved in WCS417-induced ISR showed a set of five MYB72-dependent transcripts. Among them, three genes have been reported previously to be controlled by FIT1 (Fe-deficiency Induced Transcription Factor 1), the central transcriptional regulator of the iron deficiency response in Arabidopsis roots. These three FIT- and MYB72-regulated genes encode the nitrate transporter NRT1.8, the β-glucosidase BGLU42, and the cytochrome P450 monooxygenase CYP71B5 (Zamioudis et al. 2014). Interestingly, BLU42 over-expression in Arabidopsis gives resistance to different pathogens. On the other hand, bglu42 mutant line is unable to trigger WCS417-mediated ISR. Moreover, the mutant lines myb72 and bglu42 are impaired in the accumulation and secretion of fluorescent phenolic compounds that are produced via the phenylpropanoid route and excreted in the root vicinity playing a critical role in iron acquisition by facilitating its mobilization (Zamioudis et al. 2014). The induction in MYB72 expression was also observed in plants treated with VOCs produced by WCS417, and this expression was accompanied by the induction of different genes involved in iron uptake and transport such as Iron-Regulated Transporter 1 (IRT1), Ferric Reduction Oxidase 2 (FRO2) and FIT1. Also, it has been

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shown that VOCs from other Arabidopsis native rhizospheric bacteria induced the expression of MYB72. Strikingly, the induction of iron deficiency markers (FRO2 and IRT1) was only observed when plants were inoculated with ISR-inducing bacteria, while the inoculation with similar bacteria that do not induce ISR was unable to induce the expression of iron management genes. This indicates a close relationship between the induction of ISR and the activation of iron management response (Zamioudis et al. 2015). It is important to mention that both the induction of MYB72 and the iron-related genes by VOCs is independent of the availability of iron in roots, but it is dependent on signals from above-ground parts of the plant (Zamioudis et al. 2015). Recently, it has been shown that the induction of the iron-deficiency response mediated by WCS417 does not depend on iron nutrition. In this trend, the plant growth promotion effect triggered by this bacterium was also observed under iron limitation conditions (Verbon et al. 2019). Since the response triggered in the roots by WCS417 inoculation showed to be dependent on shoot-to-root signaling, the authors evaluated if iron content in the leaves could affect this response. However, they demonstrated that iron content in the aerial parts of the plant did not affect the WCS417-induced response on roots. Also, this response was independent of the iron transport in the phloem mediated by the phloem-specific iron transporter (OPT3) (Verbon et al. 2019). Altogether, the information generated in these works confirms that the induction of ISR triggered by beneficial microbes is intimately related to an activation of the iron metabolism and this response is independent of the iron content that requires shoot-to-root signaling. More research is needed to determine the exact mechanisms involved in this process. As described early, some endophytic fungi can diminish disease symptoms caused by pathogens. This is the case of an endophyte strain of Colletotrichum tropicale that reduces the infection provoked by P. palmivora in cocoa plants (Christian et al. 2017). Recently, the authors analyzed the uptake and distribution of nitrogen in response to endophyte and pathogen inoculation by pulsing the soil with nitrogen-15 (15 N) and then tracing 15 N uptake and its subsequent distribution to whole plants and individual leaves. They demonstrated that endophyte-inoculated plants showed significantly greater 15 N uptake than endophyte-free plants. However, the total nitrogen amount did not vary in each treatment (Christian et al. 2019). Moreover, pathogen inoculation did not affect the 15 N content, but the co-inoculation with the endophyte and the pathogen showed a correlation between the 15 N content and the pathogen damage (Christian et al. 2019). These results suggest that endophyte colonization can modify nutrient acquisition and affect N distribution within plant tissues under pathogenic conditions.

2.5 Conclusions The main goal of the research in the field of biocontrol is to provide new and improved tools for the development of biotechnological products for disease management.

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Thus, the first step for novel product development is the exploration and discovery of new potential candidates as BCAs. Ultimately, the success of biocontrol relies on how well the search and screening process is done. Although there is not a unique and correct way to perform it, researchers should always keep in mind the final goal of the product. For example, looking for microorganisms to control postharvest diseases requires screening of microbes able to grow and colonize the surface of the fruits quickly to exclude pathogens. Another strategy to take into consideration is to conduct the isolation of potential candidates from the same or similar habitats that they will be used. If the BCAs were pretended to be used to control tomato diseases under greenhouse cultivation, it would be recommendable to isolate microbes from tomato plants cultivated under these conditions, so microorganisms will be better adapted. Moreover, screening should be performed in a way that mimics the conditions under which the agent will be used to increase control efficiency. Besides, ideal BCAs should be efficient in a wide range of environmental conditions. Then, it is important to test potential BCAs at field conditions during different years and climate conditions, and unless the BCAs is being intended to be used in a relatively constant environment it is important to determine to what extent environmental parameters such as temperature, moisture, and soil type affect biological control efficacy. On the other hand, understanding the mechanisms involved in the control by the BCAs will also help to develop a better and more efficient control strategy. For instance, parasitic BCAs will require the application of large doses of biocontrol microbes to ensure a population high enough to improve control. However, if the main control mechanism is the induction of resistance in the host, lower doses will be necessary. Finally, another important aspect that needs to be considered is the composition of native microbial communities where the BCAs will be inserted. Also, the modification in the communities’ structure provoked by the application of BCAs must be analyzed because unwanted effects could be originated. For example, there could be negative effects if the incorporation of biocontrol agents reduces the number of other beneficial microbes in the plant-associated communities. Nowadays, the use of nextgeneration sequencing techniques has led to a better understanding of the structure of plant-associated microbial communities, which will be essential to improve the design and application of biological control strategies. Regarding the relationship between nutrient management and biological control, the available information is scant. Certain reports relate the iron deficiency response with the induction of ISR mediated by beneficial microorganisms. Also, evidence has been provided on the uptake and distribution of nitrogen during the plant-endophytepathogen interaction. However, the mechanisms involved in these processes, as well as the true biological meaning of these responses yet to be explored for their bioefficacy in a befitting manner. Acknowledgments This work was supported by grants of Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) (PICT 2014-3718, 2014-3648, 2015-1803). A.G, F.R.R and O.A.R are members of the Research Career of CONICET. F.M.R is member of the Research Career of Comisión de Investigaciones Científicas (CIC). A.S.N is a postdoctoral fellow of CONICET.

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Chapter 3

Microbial Endophytes: Sustainable Approach for Managing Phosphorus Deficiency in Agricultural Soils Anupma Dahiya, Rakesh Kumar, and Satyavir S. Sindhu

Abstract Phosphorus (P) is the second most essential mineral nutrient after nitrogen for plant growth and development. The available form of P for plants is generally low even in fertile soils throughout the world. Phosphorus deficiency in soil is traditionally overcome by adding the phosphatic fertilizers, which also gets fixed into insoluble unavailable forms due to the high reactivity of soluble P with calcium, iron, or aluminum. The repeatedly applied fertilizer to agricultural fields led to the loss of soil fertility disturbs the soil microbial flora and causes pollution problems. Phosphate solubilizing microbial endophytes have played a significant role in phosphate solubilization. Endophytic microorganisms associated with different parts of the plants release organic acids into the soil, which solubilize the bound form of phosphate complexes and converts them into ortho-phosphate for uptake and utilization by plants. Inoculation of endophytic phosphate solubilizing microorganisms is a reliable technique for increasing soluble P in the soil leading to improved plant biomass and yield of crops. The rhizospheric bioengineering of bacterial strains to enhance phosphate solubilizing capacity will further help in improving the efficacy of biofertilizer inoculants for increasing crop productivity in sustainable agriculture. Thus, the use of plant growth-promoting bacterial endophytes as microbial biofertilizers provides a promising eco-friendly and cost-effective alternative to chemical fertilizers in sustainable agriculture. Keywords Endophytes · Plant colonization · Phosphate solubilization · Plant growth promotion · Biofertilizers

3.1 Introduction In the endophytic growth, microorganisms invade and develop close mutualistic relationships with the plants. They live in cells and tissues, and establish their interaction with different degrees of dependence, surface-sterilized plant tissues. They do not A. Dahiya · R. Kumar · S. S. Sindhu (B) Department of Microbiology, CCS Haryana Agricultural University, Hisar 125 004, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_3

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cause any noticeable symptoms to their host plants (Santoyo et al. 2016). These microbes can exist within the aboveground and underground parts of crop plants and even in the seeds, which can be isolated from surface-disinfested plant tissue or extracted from inside the plant (Hallmann et al. 1997; Chebotar et al. 2015). These endophytic microorganisms use the plant endosphere as a unique protective ecological niche that provides a safe and unperturbed environment under fluctuating conditions (Senthilkumar et al. 2011). Most of the endophytic microorganisms possess a biphasic life cycle that alternates between plants and soil environments. Thus, endophytic microorganisms are a specialized group of rhizosphere microbes that have acquired the ability to invade their plant host (Reinhold-Hurek and Hurek 2011). They share all the important traits consistent with the host plant growth promotion of beneficial rhizosphere microbes. Endophytes can communicate and interact with the plant more efficiently than rhizospheric bacteria (Ali et al. 2012; Coutinho et al. 2015). Usually, the plant growth promotion effects observed due to the inoculation of endophytic microbes to host plants are greater than those provided by many rhizospheric microorganisms. These may benefit crop plants directly by enhancing nutrient availability and may improve plant growth by modulating growth-related hormones under normal as well as stressed environmental conditions (Ma et al. 2015). Indirectly, endophytic microbes may improve plant growth by inhibiting the growth of phytopathogens using mechanisms like production of antibiotic, siderophores, lytic enzyme, and by priming plant immunity (Luo et al. 2012; Coutinho et al. 2015; Miliute et al. 2015; Maheshwari et al. 2017). Phosphorus is the second most important nutrient for the growth and development of plants after nitrogen. Plants require approximately 30 μmol l−1 of soil phosphorus for maximum productivity, but its availability is only about 1 μmol l−1 in many soils. Therefore, the unavailability of phosphorus in many soils has been recognized as a major growth-limiting factor in agricultural and horticultural systems (Daniels et al. 2009). On the other hand, the efficiency of applied phosphorus rarely exceeds 30% due to fixation as calcium, iron, or aluminum phosphates in soil (Sharma et al. 2013). Some of the phosphorus is also lost as a result of run-off and leaching (Sashidhar and Podile 2009). Thus, phosphorus deficiency in soil is traditionally overcome by adding either phosphatic fertilizers (Khan et al. 2007) or it may be incorporated as leaf litter, plant residues, or animal remains. The phosphatic fertilizers are the world’s secondlargest bulk chemical used in agriculture on earth (Goldstein 2007). After the addition of chemical phosphatic fertilizers, the extremely reactive soluble phosphate anions (H2 PO4 − , HPO4 2− ) may form metal complexes with Ca in calcareous soils (Lindsay et al. 1989) and Fe3+ and Al3+ in acidic soils (Norrish and Rosser 1983). Thus, a large portion, i.e., 75–90% of added P fertilizer in agricultural soils is precipitated/immobilized rapidly by iron, aluminum, manganese, and calcium complexes depending on soil type, soil pH, and existing minerals (Bünemann et al. 2006; Vu et al. 2008; Miller et al. 2010). Moreover, the phosphatic fertilizers are being prepared from phosphate-containing rocks, which is a non-renewable resource. The current global reserves of rock phosphates may be depleted in the next 50–100 years (Cordell et al. 2009). Therefore, endophytes having phosphate solubilization ability could

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provide phosphorus to crops. The inoculation of crops with phosphate solubilizing microbes (PSM) has the potential to reduce the application of phosphatic fertilizer without significantly reducing crop yield (Jilani et al. 2007; Yazdani et al. 2009). Recently, many phosphate solubilizing endophytes have been characterized from different plant tissues to develop effective phosphatic biofertilizers. The inoculation of these endophytes improved P solubilization capacity and resulted in increased plant growth and crop yield.

3.2 Phosphorus Availability in Soil Soil phosphorus exists either in inorganic or organic forms (Richardson 2001). Inorganic phosphorus accounts for 35–70% of total soil P (Sharon et al. 2016) and it occurs mostly in insoluble mineral complexes such as apatite, hydroxyapatite, oxyapatite, mono-, di-, and tricalcium phosphates. The organic compounds making up the humus fraction are derived from surface vegetation, microbial protoplasm, or metabolic products of the microflora. The various inositol phosphates or related substances in the organic matter frequently account for 20–80% of the entire organic P fraction. Most of the organic P sources are phytin, inositol phosphates, phospholipids, nucleic acids, sugar phosphates, polyphosphates, and phosphonates. Phosphorus held within soil microorganisms constitutes a significant component of the total soil P and is estimated to account for around 2–10% of total soil P (Achat et al. 2010). Usually, soils rich in organic matter contain abundant organic P. Moreover, a good correlation exists between the concentrations of organic P, organic C, and total N. Ratios of organic C to organic P of 100–300:1 are common for mineral soils. The soil type, soil use, and management strategies differ considerably for a proportion of different phosphorus fractions (Li et al. 2007). Besides organic P, large quantities of the inorganic forms of P occur in minerals where the phosphate is part of the mineral structure, as insoluble calcium iron or aluminum phosphates (Turan et al. 2006; Vu et al. 2008). Mineral phosphate also found related to the surface of hydrated oxides of Fe and Al, which are inadequately dissolvable and assimilable. Inorganic phosphorus (IP) in acidic soil is associated with Al and Fe compound, though in alkaline soil calcium phosphate is predominant (Khan et al. 2009). According to the compilation of about 9.6 million soil tests for available P in Indian soils, it was reported that 49.3% of areas covering different states and union territories are in a low category, 48.8% in the medium and 1.9% have high category phosphorus status (Hasan 1994). Therefore, the application of phosphatic fertilizers is unavoidable in an intensive farming system. The source of P is only from phosphatic and sulfur rocks, which are non-renewable sources and the use of phosphatic fertilizers leads to the depletion of these resources. Thus, the problem of P management in the soil is also very tricky and more than 70–90% of the applied phosphatic fertilizers get fixed in the soil rendering them unavailable for plant uptake under the ideal conditions (Holford 1997).

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3.3 Colonization of Endophytic Microbes in Tissues The endophytic colonization of plants is a complex process that requires the capacity of microorganisms to compete in the rhizosphere soil and find a niche to communicate and interact with the plant tissues. Endophytic microbes have been isolated and characterized from a diverse type of plant hosts including agronomic crops, prairie plants, plants growing in extreme environments, wild and perennial plants (Zinniel et al. 2002; Nair and Padmavathy 2014; Yuan et al. 2014). Different plant parts including roots, stems, leaves, seeds, fruits, tubers, ovules, and nodules, have the presence of endophytes but the population of endophytes is larger in the roots as compared to above-ground tissues (Rosenblueth and Martínez-Romero 2006; Senthilkumar et al. 2011). Microorganisms residing in the rhizosphere have the potential to enter and colonize the plant roots and this micro-ecosystem has been widely known as one of the primary sources for endophytic colonization (Hallmann et al. 1997). Therefore, organisms in the rhizosphere, either potentially beneficial or pathogenic, are highly competitive in colonizing plant tissues and assimilate nutrients, that possibly affect plant growth and development (Haas and Keel 2003). Endophytes employ different mechanisms to gain entry into the plant tissues (Truyens et al. 2014). They usually enter the plants through the root zone but the aerial parts of the plants, including stems, leaves, flowers, and cotyledons, may also contain endophytic microorganisms (Zinniel et al. 2002). The most common mode of entry of endophytic microbes into plant tissues is through primary and lateral root cracks, and diverse tissue wounds occurring as a result of plant growth (Sprent and de Faria 1998; Sorensen and Sessitsch 2015). The leaves (stomata) and young stems are the other sites through which endophytes may enter (Roos and Hattingh 1983) through lenticels, which are usually present in the periderm of stems and roots (Scott et al. 1996), and by germinating radicles (Gagné et al. 1987) (Fig. 3.1). Bacteria can also enter via the emergence of lateral roots or root hair cells (Huang 1986). Hallmann et al. (1997) demonstrated that entry of the endophytic bacterium Enterobacter asburiae JM22 in cotton plants was assisted by the ability of the bacterium to hydrolyze plant cell wall-bound cellulose. The endophytic colonization of the host plant by the bacteria is determined by various bacterial traits. These traits are collectively referred to as colonization traits. Moreover, endophytic colonization involves a suite of environmental and genetic factors that allow a bacterium to enter the plant endosphere (Compant et al. 2010). The colonization process involves complex communication or signaling between the microbe and the host plant particularly root. It requires recognition of specific compounds in the root exudates by the endophytic bacteria (de Weert et al. 2002; Rosenblueth and Martínez-Romero 2006). Plants produce these root exudates to interact with beneficial bacteria for their ecological advantage (Compant et al. 2005). Once inside the roots, endophytic bacteria can now systemically infect the adjacent plant tissues.

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Fig. 3.1 Entry of endophytes into plant tissues and their beneficial characteristics

3.3.1 Rhizosphere and Root Colonization Rhizosphere population can range up to 109 cfu/g of bacteria and 106 cfu/g of fungi (Foster 1988; Benizri et al. 2001). Rhizoplane population ranges from 105 to 107 cfu/g fresh weight and up to 108 bacteria/g are found on leaves (Lindow and Brandel 2003; Bais et al. 2006). The colonization of the host plant root system by the bacteria is not uniform. For example, the distribution and density of Pseudomonas fluorescens strain A6RI varied according to the root zone while colonizing tomato plants (Gamalero et al. 2003). Root colonization is controlled by different factors including root exudation patterns, bacterial attachment and motility, quorum sensing, bacterial growth rate, and minimizing competition by producing antagonistic substances and acquiring nutrients efficiently (Compant et al. 2010). The chemically diverse molecules present in the root exudates are involved in chemotaxis and attract microorganisms to the root, or in the case of endophytes, to be able to colonize the internal plant tissues. The gene expression analysis of Pseudomonas putida KT2440 competently colonizing corn rhizosphere showed that bacterial genes involved in metabolism and oxidative stress were upregulated (Matilla et al. 2007). Moreover, every endophytic microbe has a distinct colonization pattern and colonization site preferences (Zachow et al. 2010). Once these bacteria have established themselves on the root’s surfaces, they penetrate the root interior using specialized mechanisms. Furthermore, another way by which endophytic bacteria avoid being detected as a pathogen by the plant is maintaining low cell densities (2–6

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log cfu) as compared to pathogenic bacteria (7–10 log cfu) (Zinniel et al. 2002). Hence, the endophytic presence of bacteria is determined by genetic determinants that enable bacterial-plant crosstalk, leading to an active endophytic colonization process (Hardoim et al. 2008). The plant host also plays a critical role in selecting an endophytic partner where secretion of specific root exudates and a selective plant defense response are considered important factors in the selection of suitable endophytes (Rosenblueth and Martínez-Romero 2006).

3.3.2 Colonization of Aerial Plant Tissues After entry into the roots, the endophytic bacteria can spread systemically to colonize above-ground tissues. These can establish stem and leaf population densities between 103 and 104 cfu under natural conditions (Compant et al. 2010). The final sink for these specialized endophytic bacteria is leaf tissue wherein they gain entry into the leaves from the phyllosphere via leaf stomata (Senthilkumar et al. 2011).

3.4 Occurrence and Diversity of Bacterial Endophytes The earth planet has been reported to contain about 300,000 species of plants. The endophytes (bacteria and fungi) have been documented in the vast majority of plants that have been analyzed so far (Smith and Read 2008). Partida-Martínez and Heil (2011) stated that an endophyte-free plant is a rare exception and such a plant without endophytes would be more susceptible to phytopathogens and environmental stress conditions (Timmusk et al. 2011). Endophytic bacterial diversity has been reported for several plant species. The population estimates of endophytic bacteria in plants may also vary depending on the type of growth media used for isolation, growth conditions of the host plant, and method used for sterilization of plant tissue (Lodewyckx et al. 2002; Eevers et al. 2015). Moreover, cultivationdependent methods can also strongly underestimate the number of bacteria present in plant tissues (Bogas et al. 2015) because culturable bacteria usually represents only 0.001–1% of the actual endophyte counts (Torsvik and Øvreås 2002; Alain and Querellou 2009). Therefore, culture-independent methods (metagenomics) which mostly rely on the total bacterial genomic DNA extraction from plant tissues, tend to be less biased in analyzing the true endophytic diversity. The emergence of molecular techniques in microbial ecology has validated more comprehensive studies of endophyte abundance, community composition, and function using genetic analysis. A broad-spectrum of endophytic bacteria have been detected from plant tissues by using culture-independent molecular biological techniques, which assess the diversity and composition of uncovering endophytes with obligate host associations such as RFLP analysis and sequencing of rDNA or rRNA. Techniques like fluorescence in situ hybridization (FISH) have also allowed studying the endophytic bacteria in

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the natural habitat (Picollo et al. 2010). The application of molecular techniques will continue to enable extensive research on environmental factors that shape endophyte communities (Gaiero et al. 2013). Combinatorial approaches, combining both culture-dependent and culture-independent methods can increase the possibility of complete structural and functional analysis of the endophytic bacterial community of a plant (Sessitsch et al. 2004; Hallmann and Berg 2006). Sessitsch et al. (2012) observed rice’s endorhizosphere using the metagenomics approach and deciphered many traits shared by the endophytic inhabitants that might be crucial in their competence and success. The 16S-rRNA pyrosequencing approach was used in determining the composition of endophytic bacterial communities in tomato leaves (Romero et al. 2001). The endophyte communities were mainly comprised of five phyla, with Proteobacteria as the most highly represented (90%), including the classes α-, β-, and γ-Proteobacteria and later is the most diverse and dominant (Miliute et al. 2015;). Other phyla detected were Actinobacteria (1.5%), Planctomycetes (1.4%), Verrucomicrobia (1.1%), and Acidobacteria (0.5%) (Santoyo et al. 2016). However, a predominance of these phyla can vary with the type of host plant species (Bodenhausen et al. 2013; Ding and Melcher 2016). Among the most commonly isolated endophytes, bacterial genera were Bacillus, Burkholderia, Microbacterium, Micrococcus, Pantoea, Pseudomonas, and Stenotrophomonas, where Bacillus and Pseudomonas are the predominant genera (Hallmann et al. 1997; Romeo et al. 2014; Chaturvedi et al. 2016). Using PCR-based Illumina pyrosequencing, the dynamics of endophytic bacterial communities of sugar beet (Beta vulgaris L.) was analyzed with different plant genotypes and their growth stages (Shi et al. 2014). The greatest numbers of OTUs (Operational Taxonomic Units) were detected during tuber growth and rosette formation, respectively. Interestingly, 43 OTUs were common to all analyzed periods. Proteobacteria was the most abundant division, with 98% of the total microbial endophyte community being composed of Enterobacteriales, Pseudomonadales, Xanthomonadales, Rhizobiales, Sphingomonadales, Burkholderiales, Actinomycetales, and Flavobacteriales. All of them were common inhabitants of the rhizosphere and therefore, suggested that the endophyte microbiome may be a subpopulation of the rhizosphere inhabiting bacteria (Marquez-Santacruz et al. 2010; Germida et al. 1998). The occurrence of Acinetobacter sp. along with Bacillus sp. was reported in the medicinal plant Echinacea (Lata et al. 2018). Bacillus sp. such as B. pumilus, B. subtilis, and B. megaterium were isolated from the roots of medicinal plant Chlorophytum borivilianum (Safed musli) and demonstrated as the major contributors to the endophytic bacterial diversity in medicinal plants (Panchal and Ingle 2011). Apart from medicinal plants, the endophytic occurrence of Acinetobacter and Bacillus species have also been reported in other crops like soybean (Li et al. 2008), sugarcane (Velázquez et al. 2008), the grapevine (Trotel-Aziz et al. 2008), sweet corn, and cotton (McInroy and Kloepper 1995; Joe et al. 2016). Gagne-Bourgue et al. (2013)

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characterized 31 indigenous and culturable bacterial endophytes from three switchgrass leaf cultivars: (Cave-in-Rock, Blue Jacket, and Tecumseh). Bacterial endophytes were identified as Microbacterium testaceum, Curtobacterium flaccumfaciens, Bacillus subtilis, Bacillus pumilus, Pseudomonas fluorescens, Sphingomonas parapaucimobilis, Serratia sp., and Pantoea ananatis. Various positive attributes viz. high biomass production, efficient water use, relatively low demand for nutritional inputs, and less use of agrochemicals were also reported in these endophytes that contributed to the adaptation of switchgrass leaf cultivars to marginal soils (Sanderson et al. 2006). Kang et al. (2018) isolated 30 endophytic and non-endophytic isolates from Medicago sativa. Other plant growth-promoting traits such as phosphate solubilization and production of indole-3-acetic acid (IAA) were also exhibited by most of the tested strains during colonization of plant tissues and soil. Schmidt et al. (2018) isolated endophytes from Miscanthus x giganteus. Genera Pantoea ananatis and Pseudomonas savastanoi exhibited as the predominant bacteria in leaves, whereas other pseudomonads prevailed in roots. Chinnaswamy et al. (2018) isolated Gram-positive, endophytic bacterium B. megaterium NMp082 from root nodules of Medicago polymorpha. The isolate co-inhabited nodules with the symbiotic Ensifer medicae, the nif H and nodD genes in the B. megaterium NMp082 were 100% identical to those of Ensifer meliloti. Although the endophyte possessed nodulation and nitrogen fixation genes, the bacterium failed to form effective nodules. However, it induced nodule-like unorganized structures in alfalfa roots. Many fungi belonging to different groups have also been reported as plant endophytes. The first group includes fungal species with a broad range of host plants, and the second group includes a smaller number of specialized fungal species that colonize some monocotyledonous hosts. Most of the endophytic fungi belong to the phylum Ascomycota and Glomeromycota whereas some fungi belong to phylum Basidiomycota and Zygomycota. The fungi from the genera Acremonium, Alternaria, Chaetomium, Cladosporium, Cryptocline, Cryptosporiopsis, Leptostroma, Phoma, Phomopsis, Phyllosticta, and Trichoderma are well represented in endophyte assemblages. Fungal endophytes within the host may inhabit different tissues of roots, stems, branches, leaves, flowers, fruits, seeds, twigs, bark, and petioles, including xylem of all available plant organs. These endophytes are classified into four classes. Class 1 endophytes form systemic associations with the aboveground tissues of grasses and are defined as the Claviciptaceous endophytes (including Balansia spp. and Epichloe spp.) (Johnson et al. 2013). These species are one of the most economically important examples of plant–endophyte interactions. The diverse class 2 endophytes include both Ascomycota and a few Basidiomycota. Their most exclusive characteristic is the ability to colonize roots, stems, and leaves, and form extensive plant infections. Class 3 comprises endophytes that form highly localized infections in aboveground tissues, such as in the leaves of tropical trees and non-vascular and vascular plants. The dark septate endophytes (DSE) constitute class 4 and these facultative biotrophic fungi colonize plant roots and have the distinguishing feature of having melanized dark septate hyphae (Jumpponen 2001; Rodriguez et al. 2009; Lugtenberg et al. 2016). Fungal endophytes play a major role in habitat adaptation

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of plants resulting in improved plant performance and plant protection against biotic and abiotic stresses. Besides, the host plant, environmental factors have been found to strongly influence the endophytic diversity of a particular plant. Moreover, host plant age, genotype, geographical location, and even the tissue being analyzed can determine the type of endophytic bacteria it harbors (Hallmann and Berg 2006). Besides this, host plant growth stages can also determine the endophytic diversity of a plant, where plant stages enriched in nutrient availability tend to have increased bacterial diversity (Shi et al. 2014). Climatic conditions have also been reported to influence the endophytic colonizers of a plant species. Earlier, Penuelas et al. (2012) reported that changes in a climate significantly altered the abundance and composition of endophytic bacteria within the leaf tissues. Different plant species growing in the same soil can have distinctly different endophytic diversity, suggesting that the type of endophytic community of a plant is strongly influenced by the nature of the plant host species (Ding et al. 2013; Ding and Melcher 2016). Germida et al. (1998) reported that canola and wheat plants grown in the same field had a very different spectrum of bacterial species as endophytes. Even the different cultivars of a plant species grown in the same soil can also differ in their endophytic diversity. Graner et al. (2003) reported that four different cultivars of Brassica napus possessed different endophytic bacterial inhabitants. Song et al. (1999) also reported significantly different endophytic bacterial diversity for peanut cultivar grown in different fields. Moreover, Rashid et al. (2012) isolated different types of endophytic bacteria by growing one cultivar of tomato in 15 different agricultural soils. Similarly, Graner et al. (2003) reported that wilt resistant cultivar of Brassica napus contained a higher proportion of endophytic bacteria antagonistic to the wilt-causing Verticillium longisporum than the susceptible cultivar. The restructured endophytic communities of asymptomatic and symptomatic Paullinia cupana plants were observed when challenged by Colletotrichum spp. Bogas et al. (2015), suggested that the presence of phytopathogens in plants is an important factor in the restructuring of endophytic bacterial communities. Hence, the selection of endophytic bacterial communities is a dynamic process that is tightly controlled by the host plant (Berg and Hallmann 2006; Trivedi et al. 2010).

3.5 Phosphorus Solubilization by Endophytic Microorganisms The mechanisms of plant growth promotion employed by endophytic microorganisms are similar to the mechanisms used by rhizospheric bacteria. Endophytic microbes help in the acquisition of nutrients for plant growth and development. The main difference being that endophytic microbes are no longer subject to the vagaries of changing soil conditions, once they have been established within the tissues of the host plant, These changing conditions include variations in temperature, soil pH,

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and water content, and the presence of soil bacteria that may compete for binding sites and nutrients on host plant root surfaces (Glick 2012; Sindhu and Dadarwal 2000). Endophytic bacteria have been shown to impart several beneficial effects on their plant host directly or indirectly. They can benefit plants directly by assisting plants in getting nutrients and improve plant growth by modulating growth-related hormones, which can help plants grow better under normal and stressed conditions (Ma et al. 2016) and indirectly by the improvement of plant growth due to inhabition of phytopathogens (Miliute et al. 2015). Nitrogen, phosphorus, and potassium are usually available in limited quantities for plant growth in agricultural soils. The endophytic bacteria help their host plants in getting increased amounts of limiting plant nutrients (Glick 2012). Endophytic bacteria have been found to contribute toward solubilization of phosphate, potassium, and zinc, and also provide fixed nitrogen and plant growth-promoting substances to the host plants under a wide range of environmental conditions. These bacteria release certain organic acids such as citric acids, oxalic acid, gluconic acid, lactic acid, fumaric acid, etc., which contribute toward solubilization of bound phosphorus in soil. Numerous genera with the ability to solubilize phosphorus and synthesize auxins include Pseudomonas, Bacillus, Rhizobium, Xanthomonas, Serratia, Piriformospora, Burkholderia, Achromobacter, Agrobacterium, Micrococcus, Flavobacterium, Erwinia, Enterobacter, and Paenibacillus (Whitelaw 2000; Fraga et al. 2001; Mota et al. 2008; Ribeiro and Cardoso 2012). Phosphorous is the second most abundant plant nutrient after nitrogen, which is crucial for enzymatic reactions responsible for different plant physiological processes (Sindhu et al. 2014; Ahemad 2015). The majority of the soil phosphorus is insoluble, therefore, it cannot support the plant growth due to its unavailability. Moreover, almost 75% of phosphorus applied as fertilizer forms complexes with iron, aluminum, and calcium in the soil and becomes unavailable for the plants (Ezawa et al. 2002). Phosphorus deficiency causes stunted growth, forms dark leaves, causes inhibition of flowering, and adversely affects the development of the root system. Phosphorus compounds in the soil can be present in bound forms either as: (i) inorganic compounds, (ii) organic compounds of the soil humus, and (iii) organic and inorganic P compounds associated with the cells of living matter. Mineral compounds of P usually contain aluminum (Al), iron (Fe), manganese (Mn), and calcium (Ca) and vary in different kinds of soils. For example, under acidic conditions phosphorus forms a complex with Al, Fe, and Mn, where as it reacts very strongly with Ca in alkaline soils (Khan et al. 2014). Thus, the applied P fertilizers are easily precipitated into insoluble forms, i.e., CaHPO4 , Ca3 (PO4 )2 , FePO4 , and AlPO4− , and are not efficiently taken up by the plants, which lead to an excess application of P fertilizer to achieve maximum plant productivity (Omar 1998). These agricultural practices disrupted natural ecological nutrient cycling, health hazards, environmental disturbance, and damage to biological communities. Many endophytic microorganisms enhance the availability of phosphorus for plants by solubilization of precipitated phosphates (Nautiyal et al. 2000; Zhao et al. 2015; Adhikari and Pandey 2019) (Table 3.1). These microorganisms increase phosphorus availability in the soil either by secreting acid phosphatase that can mineralize

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Table 3.1 Phosphorus-solubilizing endophytic microorganisms Species

Microorganisms involved

Bacteria

Bacillus megaterium, B. circulans, B. subtilis, B. polymyxa, B. sircalmous, Pseudomonas striata, Pseudomonas sp., Enterobacter sp., Enterobacter cloacae, Beggiatoa, Thiomargarita sp., Leifsonia xyli, Burkholderia cenocepacia, Burkholderia caribensis, Burkholderia ferrariae, Achromobacter, Acinetobacter, Pantoea agglomerans

Actinobacteria Actinobispora yunnanensis, Actinomodura citrea, Microtetrospora astidiosa, Micromonospora echinospora, Sacchromonospora viridis, Saccharopolyspora hirsute, Streptomyces albus, Streptoverticillium album, Streptomyces cyaneus, Thermonospora mesophila Fungi

Aspergillus awamori, Fomitopsis sp., Penicillium bilaii, Piriformospora indica, dark septate endophytes

Mycorrhiza

Glomus, Funneliformis, Rhizophagus, Sclerocystis, Claroideoglomus, Gigaspora, Scutellospora, Racocetra, Acaulospora, Entrophospora, Pacispora, Diversispora, Otospora, Paraglomus, Geosiphon, Ambispora, Archaeospora sp.

organic phosphorus (Van Der Heijden et al. 2008) or by the release of organic acids that solubilize the bound phosphorus (Fig. 3.2). Moreover, endophytic bacteria can prevent phosphate adsorption and fixation under phosphate limiting conditions by

Fig. 3.2 Different mechanisms employed by microbes for phosphate solubilization

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assimilating solubilized phosphorus (Khan and Joergensen 2009). Thus, endophytic bacteria can act as a sink to provide need-based phosphorus to the plants.

3.5.1 Phosphate Solubilization by Endophytic Bacteria Phosphate solubilization feature is commonly found in endophytic bacteria. About 59–100% of endophytic populations obtained form cactus, strawberry, sunflower, soybean, and other legumes were found to possess the ability to solubilize phosphate (Kuklinsky-Sobral et al. 2004; Forchetti et al. 2007; Dias et al. 2009; Puente et al. 2009a; Palaniappan et al. 2010). The role of phosphate solubilizing endophytic bacteria was established by growing bacteria-free cacti on mineral phosphate supplemented with either endophytes or nutrients, and these plants were compared with plants grown under sterile conditions (Puente et al. 2009b). The growth of inoculated plants without nutrient addition was comparable to the fertilized plants, whereas the bacteria-free unfertilized cacti failed to grow. These results suggested that endophytic bacteria provided the developing plantlets with the limiting nutrient phosphorus. Longback, Gaur (1990) observed a gradual increase of available P and acidity of the medium up to a certain period by Pseudomonas striata, the available P level corresponded with an increase of pH to a certain extent. Many phosphate solubilizing microbes are responsible for the production of organic acids and gluconic acid is known as the principal organic acid for mineral phosphate solubilization.. The highest phosphate solubilization capacity was observed in isolates EB-47 and EB-64 (Bacillus sp. and Bacillus pumilus). The isolate EB-53 (Lysinibacillus sp.) showed high solubilization index, whereas 73% of the isolates showed low solubilization indices. These endophytic bacteria were subsequently used as growthpromoting microbial inoculants in nurseries growing banana suckers (Andrade et al. 2014). Endophytic isolates of P. fluorescens were obtained from the silver grass (Miscanthus giganteus) crop (Oteino et al. 2013). Maximum phosphate solubilization was recorded in P. fluorescens strain L228 and Pseudomonas sp. strain L132 in comparison to negative control E. coli JM109. All strains showed the production of gibberellic acid (GA) with a concentration ranging from 2840 to 33240 ± 230 mg L−1 (14–169 mM). Kumar et al. (2013) isolated root endophytes from nodules of legume plants. Large numbers of Gram-positive bacterial endophytes were present in legume nodules than in its roots, which showed 56 and 47.8% phosphate solubilizing ability, respectively. From legume roots, 56.9% isolates showed phosphate solubilizing activity, whereas only 35.9% showed from non-legume roots. Moreover, the highest numbers of phosphate solubilizing isolates (73.3%) were observed from field pea roots and the lowest numbers of phosphate solubilizing isolates (20%) were observed in oat roots. The amount of P solubilization was higher in isolates from chickpea than oat roots. The significant phosphate solubilizing bacterial isolates were obtained from legume roots and nodules (CRE1 and CNE215) and non-legume roots (WRE10, WRE20, and

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ORE35). Isolate ORE35 was the most potential P solubilizers among all these endophytic isolates. Three promising isolates were identified by 16S rRNA sequencing for instance from chickpea nodules B. subtilis strain CNE215; whereas roots have B. licheniformis strain CRE1; in case of wheat root B. flexus strain WRE 20. B. methylotrophicus strain CKAM was selected from the root endosphere of healthy apple trees based on higher P-solubilization (687 mg/L) and other plant growth-promoting attributes (Mehta et al. 2014). Five rhizospheric and two root endophytic actinobacteria were isolated from wheat plants (Jog et al. 2014). Maximum phosphate solubilizing activity in tricalcium phosphate supplemented medium was exhibited by actinobacterial isolate Streptomyces mhcr 0816. Zhao et al. (2015) isolated 48 endophytic bacteria from surface-sterilized tissues of the medicinal plant Lonicera japonica wherein few isolates showed a zone of phosphate solubilization on the Pikovskaya agar medium. These bacterial strains were identified as Paenibacillus and Bacillus strains. Pandya et al. (2015) isolated 26 non-rhizobial and one fungal endophyte from Vigna radiata root nodules and only 11 endophytes solubilized phosphate. Maximum phosphorus solubilization was observed in Paenibacillus xylanilyticus strain M15 (134.483 μg ml−1 ). The free phosphate release ranged from 37.4 μg ml−1 in strain M13 to 134.48 μg ml−1 in the strain M15. However, free phosphate released by strain M15 was significantly lower than free phosphate released by the endophyte B. cereus strain P31 (354.3 μg ml−1 ) isolated from potato roots (Dawwam et al. 2013). The most efficient phosphate solubilizing strains belong to species of Klebsiella (M13), Dyadobacter, Blastobacter, Bacillus, and Paenibacillus spp. Bacterial endophytes were also isolated and characterized from the root and shoot tissues of Lavandula dentate plants growing under organic management (Pereira et al. 2016). These were identified as Pseudomonas brassicacearum subsp. neoaurantiaca, Pseudomonas moorei, Variovorax soli, Pseudomonas frederiksbergensis, Pseudomonas fuscovaginae, B. cereus, Bacillus aerophilus, Bacillus drentensis, Pseudomonas graminis, Bacillus aryabhattai, and Pseudomonas lutea. The higher bacterial diversity of endophytes was observed in roots having to six different genera (Pseudomonas, Variovorax, Rhizobium, Caulobacter, Bacillus, and Paenibacillus), while in shoots, 91% of the endophytic isolates were characterized and identified as Bacillus and Pseudomonas, whereas only one belongs to genus Xanthomonas. Matos et al. (2017) isolated 40 endophytic bacterial isolates from banana tree roots. Approximately 67.5% of the isolates solubilized phosphorus from soy lecithin. Acid phosphatase activity was detected in 65% of the isolates and Aneurinibacillus sp. and Lysinibacillus sp. isolates showed the best solubilization indexes. Bacillus sp. isolate EB78 exhibited P solubilization capacity in solid media when Ca3 (PO4 )2 and soy lecithin were used as P sources. This isolate significantly reduced the pH of the liquid medium and exhibited acid phosphatase activity. The salt-tolerant endophytic and phosphate solubilizing bacterial isolates Acinetobacter sp. ACMS25 and Bacillus sp. PVMX4 was isolated from Phyllanthus amarus (Govindasamy et al. 2018). These isolates showed a higher zone of clearance and solubilization index when compared with standard B. megaterium strain MTCC446 in the presence of 160 mM NaCl (Chen et al. 2006; Tao et al. 2008; Verma et al. 2013).

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Kshetri et al. (2018) isolated Arthrobacter luteolus S4C7, Enterobacter asburiae S5C7, Klebsiella pneumoniae S4C9, S4C10, and S6C1, and K. quasipneumoniae S6C2 from the rhizosphere of Allium hookeri. All the isolates released a substantial amount of soluble phosphate.

3.5.2 Phosphate Solubilization by Endophytic Fungi Several rhizospheric fungi such as arbuscular mycorrhizal (AM) fungi support plant mineral nutrition in exchange for photosynthetic carbon and colonize the root zone (Smith and Read 2008). The root endophytic fungus Piriformospora indica, which is an anamorphic strain of the Sebacinales (Basidiomycota) was isolated from the Thar Desert of India (Verma et al. 1998). P. indica can colonize roots and promote plant growth independent of phosphate concentrations in the soil (Yadav et al. 2010). Nath et al. (2012) isolated P-solubilizing endophytic Penicillium species from tea leaves which showed significant phosphate solubilizing activity with an increase of acidity of the medium. The decrease in the pH of the medium was associated with an increased amount of available P in the medium. Dark septate endophytes (DSE) are root colonizing soil fungi, which establish a wide range of symbiotic interactions with the host plants. Occurrence of these fungi has been associated with more than 600 plant species, including non-mycorrhizal plants (Mandyam and Jumpponen 2005; Sieber and Grünig 2006). They can grow in both biotrophic and saprophytic ways, hence have different effects on their hosts (Mandyam et al. 2012). Barrow and Osuna (2002) showed that Aspergillus ustus (DSE strain) can solubilize soil phosphate and increase P availability to Atriplex canescens (Hernandez et al. 2011; Rinu and Pandey 2010). Bashan et al. (2013) isolated DSE fungi from wheat (T. aestivum) and two forages (Panicum coloratum and Chloris gayana) which solubilized calcium, aluminum, and iron phosphates, in vitro methodologies. Rinu et al. (2013) reported that the carbon and nitrogen sources can influence the phosphate solubilizing efficiency of the fungi. Comparatively, the efficiency of the strain of Ophiosphaerella sp. was found similar to that of the filamentous fungus Paecilomyces lilacinus. Spagnoletti et al. (2017) isolated dark septate endophytes from the roots of wheat (Triticum aestivum) and forage crops Panicum coloratum and Chloris gayana, grown in slightly acidic and alkaline soils of Argentina. The isolates showed the ability to solubilize calcium phosphate, three strains solubilized aluminum phosphate, and none of them solubilized iron phosphate on solid media. Maximum calcium phosphate solubilization was carried out by Ophiosphaerella sp., Cochliobolus sp., and Setosphaeria rostrata. Endophytic strains Drechslera sp. and Ophiosphaerella herpotricha showed maximum aluminum phosphate solubilization. Priyadharsini and Muthukumar (2017) isolated Curvularia geniculata, a dark septate endophytic fungus from Parthenium hysterophorus L. to solubilize different sources of phosphorus.

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Recently, Adhikari and Pandey (2019) isolated endophytic fungi of genera Penicillium and Aspergillus from the roots of Taxus wallichiana. The endophytes solubilized phosphate by utilizing the substrates, namely, calcium, aluminum, and iron phosphate along with the production of phosphatase and phytase enzymes. Maximum phosphate solubilization and phytase activity were recorded in P. daleae, which produced maximum calcium phytase. The phosphatase activity was higher in acidic conditions in comparison to alkaline conditions due to release of different organic acids.

3.6 Beneficial Traits of Endophytic Microorganisms Some of the phosphate solubilizing endophytes have also been found to possess other beneficial traits, i.e., nitrogen fixation, hormone production, growth inhibition of phytopathogenic fungi, stress amelioration by reduction of ethylene concentration by the production of ACC deaminase, and solubilization of metals in the soil.

3.6.1 Nitrogen Fixation by Endophytes The endophytic bacteria of the genera Gluconacetobacter diazotrophicus, Herbaspirillum seropedicae, H. rubrisubalbicans, Azotobacter, Beijeinckia, Methylobacterium, and Azospirillum showed nitrogen fixation capacity in different cultures with nonleguminous plants and have been used as a prominent alternative of nitrogen fertilizers (Cavalcante et al. 2007). Endophytic bacteria increase the nitrogen availability for their host plants. These bacteria can supply fixed atmospheric nitrogen to their host plants by expressing nitrogenase activity (Montanez et al. 2012). Nitrogenfixing bacteria like Azoarcus sp. BH72, Azospirillum brasilense, Burkholderia spp., Gluconacetobacter diazotrophicus, and Herbaspirillum seropedicae have also been reported to increase the host plant biomass by N2 fixation under controlled conditions (Bhattacharjee et al. 2008). Strains of G. diazotrophicus have been identified living in symbiosis with sugarcane and pine plants (Carrell and Frank 2014). Shabanamol et al. (2018) obtained nitrogen-fixing endophytic diazotrophic isolates from surface-sterilized leaf, stem, and root samples of various rice cultivars using Dobereiner’s semisolid N free bromothymol blue media. Associative nitrogen-fixing endophytes perform better than rhizosphere microorganisms in enabling plants to thrive in nitrogen-limited soil environments and promoted plant health and growth (Hurek and Reinhold-Hurek 2003). Nitrogen-fixing endophyte Paenibacillus strain P22 has been found in a poplar tree, and have been demonstrated to contribute to the total nitrogen pool of the host plant (Scherling et al. 2009). Gupta et al. (2013) reported that endophytic nitrogen-fixing bacteria may also enhance the rate of nitrogen fixation and accumulation in plants residing in nitrogen-limited soils but these are not as efficient as root nodule associated Rhizobium in nitrogen fixation ability.

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3.6.2 Phytohormone Mehta et al. (2014) obtained endophytic P-solubilizing rhizobacteria from 20 healthy apple roots and found that endophyte B. methylotrophicus CKAM obtained from root endosphere showed the higher phosphate solubilization (on PVK agar plates in vitro). B. methylotrophicus also showed nitrogenase activity, IAA, siderophore, and antifungal activity against F. oxysporum, Phytophthora sp., D. necatrix, S. rolfsii, and P. aphanidermatum. Pirhadi et al. (2018) isolated bacterial endophytes from roots, stems, and leaves of sugarcane grown in saline and non-saline soil. The authors observed a prevalence of Bacillaceae, with Bacillus sp. being the most frequently isolated bacterium and salinity affected the bacterial community structure and higher diversity of root entophytic P-solubilizing bacteria. Earlier, Kruasuwan and Thamchaipenet (2016) reported that bacterial endophytes isolated from sugarcane rhizosphere exhibited plant growth-promoting traits especially indole-3acetic acid, nitrogen fixation, ACC deaminase, phosphate solubilization, siderophore production, etc. Shabanamol et al. (2018) observed that three diazotrophic isolates inhibited the growth of rice sheath blight pathogen Rhizoctonia solani, also produced indole-3-acetic acid, gibberellic acid, and cytokinins. Ribeiro et al. (2018) reported that Bacillus strains produced high levels of IAA in the presence of tryptophan. Sun et al. (2019) observed that the production of indole acetic acid significantly enhanced root biomass and root–shoot ratio on medicinal plant Astragalus mongholicus.

3.6.3 Endophytic Microbes as a Biocontrol Agent A few endopytic microorganisms also act as potential biocontrol agents. An endophytic bacteria Pantoea vagans C9-1 was commercialized as a bacterial biocontrol agent for fire blight (Smits et al. 2011). Aravind et al. (2009) reported for suppression of phyto-parasitic burrowing nematode (Radopholus similis Thorne) by endophytic bacteria Bacillus megaterium BP17 and Curtobacterium luteum TC10. Similar to B. thuringiensis, endophytic bacteria active against plant pests have also been demonstrated, where genetically modified endophytic P. fluorescens expressing Bacillus thuringiensis toxin and Serratia marcescens chitinase effectively targeted Eldana saccharina (sugarcane borer) larvae (Downing et al. 2000). Niu et al. (2011) showed that B. cereus AR156 triggered both the SA and JA/ET signaling pathways in Arabidopsis to induce ISR, which led to an additive effect of plant protection. Earlier, similar to the above studies, Conn et al. (2008) indicated that A. thaliana plants inoculated with endophytic actinobacteria showed upregulation of both defense pathways, thereby protecting against subsequent infection by phytopathogenic bacteria E. carotovora and fungus F. oxysporum. However, the primed defense pathways differed for the two pathogen types. The resistance to E. carotovora involved JA/ET pathway, while resistance toward F. oxysporum was mainly followed the SA pathway. It is

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interesting to note that the same bacterium was able to prime two different pathways to confer resistance to the different pathogens (Conn et al. 2008). Mehta et al. (2014) reported that phosphate solubilizing endophytic bacteria showed maximum antagonistic effect against S. rolfsii followed by F. oxysporum, D. necatrix, P. aphanidermatum, and Phytophthora sp. by producing various antifungal compounds such chitinase, proteases, pectinase, and the antibiotic lipopeptides surfactin, fengycin, and iturin A. Shabanamol et al. (2018) reported that three diazotrophic isolates, showed in vitro antifungal activities against rice sheath blight pathogen R. solani. All the isolates produced IAA, GA, and cytokinins. Morphological, physiological, biochemical characteristics, and 16S rDNA sequence analysis identified the isolates as Lysinibacillus sphaericus, Klebsiella pneumonia, and Bacillus cereus. Endophytic bacteria Pseudomonas stutzeri strain E25 and Stenotrophomonas maltophilia strain CR71 produced volatile compound dimethyl disulfide, which exhibited significant antifungal activity against Botrytis cinerea (Rojas-Solis et al. 2018). Recently, Manganyi et al. (2019) determined the antimicrobial metabolites produced by endophytic fungi Sceletium tortuosum L. The endophytic fungi produced secondary metabolites that displayed a narrow spectrum of activity against the bacterial strains. None of the fungal extracts inhibited the growth of Enterococcus faecalis (ATCC S1299) and Enterococcus gallinarum (ATCC 700425) while Bacillus cereus (ATCC 10876) was the most susceptible agent against the fungal extracts. In general, Fusarium oxysporum (GG 008) displayed significance because it was linked to high levels of 5-hydroxymethylfurfural (HMF) and octadecanoic acid as revealed by GC-MS.

3.6.4 Endophytes in ACC Deaminase and Stress Amelioration As a consequence of the presence of an ACC deaminase-containing organisms, a plant that has been exposed to either biotic or abiotic stress conditions may be partially or even completely protected from the ethylene inhibition of plant growth (Glick 2014). Thus, ACC deaminase-containing microbes effectively protect against growth inhibition by flooding, high salt, drought, against fungal and bacterial pathogens, nematode damage, the presence of high levels of metals and organic contaminants, as well as low-temperature stress condition (Khandelwal and Sindhu 2012; Glick 2015). Involvement of ACC deaminase in endophytic plant growth promotion was reported in Burkholderia phytofirmans PsJN (Sessitsch et al. 2005). The mutants of this bacterium lacking ACC deaminase activity were no longer able to promote canola seedling root elongation (Sun et al. 2009). Besides, two of these ACC deaminaseproducing endophytic PGPB (compared to ACC deaminase minus mutants of the same strains) have also been tested for the ability to promote tomato plant growth in the presence of very high levels of salt and to delay the senescence of mini carnation cut flowers (Ali et al. 2012). ACC deaminase-producing endophytic PGPB were

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readily taken up through the stems of cut flowers, subsequently delaying flower senescence by several days (Ali et al. 2012). The endophytic bacterium B. megaterium NMp082 isolated from root nodules of Medicago polymorpha reported to exhibit ACC deaminase activity in vitro and its inoculation promoted growth in M. polymorpha, Medicago lupulina, Medicago truncatula, and Medicago sativa. B. megaterium NMp082 also induced tolerance to salt stress in alfalfa and Arabidopsis plants (Chinnaswamy et al. 2018).

3.6.5 Metals Solubilization by Endophytes Soil contamination with heavy metals due to anthropogenic activities such as mining, combustion of fossil fuel, agrochemicals, and sewage sludge has become one of the most severe environmental hazards throughout the world. Interactions between plants and beneficial microorganisms have received much attention worldwide for the bioremediation and phytoremediation of polluted sites as a cleaning technology for removing metals from soils. Pereira and Castro (2014) isolated distinctive microbial communities from woody tree species to herbaceous crop plants, which showed predominant existence in all higher plants (Luo et al. 2011) and able to colonize different plant compartments such as roots, stem, leaves, flowers as well as fruits and seeds (Compant et al. 2011; Sun et al. 2010). These endophytes may act as bioinoculants in the recovery of metal contaminated soils, constituting a biological alternative to improve phytoremediation efficiency. Several bacterial endophytes were isolated from the Zn/Cd hyperaccumulator plant Sedum plumbizincicola (Ma et al. 2015; Ullah et al. 2015). On the other hand, the effect of the rhizobial endosymbiont Sinorhizobium meliloti strain CCNWSX0020 under copper stress was recently evaluated (Kong et al. 2015). This strain increased both plant growth and nitrogen content. Besides, the rhizobial symbiosis promoted Cu accumulation in plant shoots and roots. Also, several plant genes involved in antioxidant responses were upregulated in plants treated with the bacterium in the presence of high levels of Cu. Thus, the symbiosis with S. meliloti not only enhanced plant growth and metal uptake but also induced the plant’s antioxidative defense responses under Cu stress. Verma et al. (2014) isolated endophytic bacteria Delftia and Micrococcus from wheat and six percent isolates showed the highest potassium (K) solubilization, i.e., some other bacterial genera such as Stenotrophomonas maltophilia and IARI-IIWP27 Pseudomonas monteilii also showed significant K-solubilization. Wagh et al. (2016) found that two endophytic microorganisms Hs (pJNK5) and Hs (pJNK6) of species H. seropedicae that showed K-solubilization on Aleksandrov agar plates.

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3.7 Inoculation Responses of Endophytes on Plants Numerous reports exist regarding the application of endophytic bacteria in the growth promotion of wheat, rice, canola, potato, tomato, etc. (Mei and Flinn 2010; Sturz and Nowak 2000) (Table 3.2). Most of the studies involve the growth promotion potential of the endophytes isolated from the same plants or the plants which are very closely related to their natural host (Long et al. 2008). However, some endophytic bacteria have been reported to cause growth promotion on non-host or diverse host plants (Sessitsch et al. 2005; Ma et al. 2011), indicating contrasting observations about the host specificity of endophytes. The broad-host-range of endophytes makes a powerful tool in agriculture biotechnology and, therefore, endophytes have a great potential to be used as biofertilizers and biopesticides in sustainable agrobiological practices. Our understanding of endophyte communities and the ability to predict the success of endophytes to promote plant growth under field conditions is limited. Various soil, plant, and microbial factors have been reported to affect the survival, colonization, and compatibility of the endophyte to survive within the root. Moreover, the plant growth-promoting ability of endophytic microbes can be influenced by the genotype of the plant host. Bacterial genotype has been found to strongly influence the growth-promoting effects on host plants. Trognitz et al. (2008) demonstrated that different strains of B. phytofirmans differed markedly in their abilities to promote the growth of the same potato cultivar. Few decades back, Dong et al. (1994) reported that four strains of endophytic Salmonella enterica colonized alfalfa roots and hypocotyl differently. Hence, plant colonization and growth promotion by the endophytic bacteria are controlled by the genetic factors of both partners. Long et al. (2008) observed that PGP bacteria of Solanum nigrum proved highly host-specific, where these bacteria were unable to produce growth enhancement in Nicotiana attenuate, a non-host plant. However, the broad-host-range of endophytic bacteria has been demonstrated in the case of B. phytofirmans PsJN, isolated from onion roots (Pillay and Nowak 1997), which can promote the growth of A. thaliana, grape, maize, potato, switchgrass, tomato, and wheat (Sessitsch et al. 2005; SheibaniTezerji et al. 2015). Also, Thomas and Upreti (2014) demonstrated that endophytic bacterial isolates of crop plants could inhibit wilt pathogen Ralstonia solanacearum and also suppressed the disease effects of Ralstonia solanacearum on a non-host tomato plant. Moreover, endophytic bacteria from tomato grown in different agricultural soils, were able to promote canola growth under gnotobiotic conditions (Rashid et al. 2012). Afzal et al. (2015) showed that endophytic bacteria selectively isolated from Cannabis sativa rhizosphere induced growth promotion of canola. Thus, these reports suggested that endophytic bacteria have a broad-host-range potential in plant growth and development. Earlier, Wu and Guo (2008) observed that inoculation of Saussurea involucrata with a DSE fungus promoted plant growth and especially plant height similar in case of DSE inoculation in pigeon pea. Fakhro et al. (2010) inoculated tomato with Penicillium indica and observed the colonization of tomato roots by P. indica. The inoculation resulted in increased biomass of the leaves up to 20% and also reduced the

Source Root exudates Leaves

Root, stem, and leaf

Stems and roots Roots and stems Stems and fruits

Twigs and leaves Roots, stem, and leaves

Roots, stems, and leaves

Endophytic species

Azorhizobium caulinodans, Azospirillum brasilense and Serratia spp.

Bacillus, Methylobacterium, Delftia, Stenotrophomonas, Microbacterium, Paenibacillus and Staphylococcus

Bacillus and Paenibacillus

Bacillus pumilus, B. subtilis, Pseudomonas aeruginosa and P. fluorescens

Serratia sp., S. marcescens, Klebsiella sp., K. variicola and Stenotrophomonas sp.

Pseudomonas sp. and Brevibacillus brevis

Bacillus sp. and Pantoea sp.

B. cereus, B. licheniformis, Bacillus sp, Burkholderia gladioli, Paracoccus halophilus, and Stenotrophomonas sp.

Enterobacter ludwigii, Pantoea agglomerans, and Variovorax paradoxus

Table 3.2 Inoculation effect of endophytic bacteria on different hosts

Isolates showed IAA production, phosphate solubilization and plant growth promotion in soybean

Endophytes promoted plant growth and 50–64% enhanced biomass accumulation of tomato

Enhanced seedling growth in rice

Production of phytohormones, antifungal activity, chromium tolerance, phosphate solubilization, and PGPR activity in tomato

Plant growth promotion in rice

Effect on population densities in maize

Deformity of fungal mycelia, IAA and siderophore production, ACC utilization, phosphate solubilization, increase in shoot length, root length, fresh weight, dry weight, and chlorophyll content in wheat seedlings

Biological control of plant diseases and plant growth promotion in common bean

ACC deaminase production, stress reduction, and increased root growth in wheat and rice

Effect on plant

(continued)

de Almeida Lopes et al. (2016)

Xia et al. (2015)

Deivanai et al. (2014)

Patel et al. (2012)

Mbai et al. (2015)

Rai et al. (2007)

Zhao et al. (2015)

Costa et al. (2012)

Hardoim et al. (2008)

References

54 A. Dahiya et al.

Source Seed

Rhizome tissues

Roots

Endophytic species

Flavobacterium sp., Pseudomonas sp., Microbacterium sp., and Xanthomonas sp.

Serratia, Enterobacter, Acinetobacter, Pseudomonas, Stenotrophomonas, Agrobacterium, Ochrobactrum, Bacillus and Tetrathiobacter

Enterobacter and Pseudomonas

Table 3.2 (continued)

Mn tolerance, antifungal activity, ammonia and IAA production in chickpea

IAA production, N, P, and K uptake, plant height, leaf area, and biomass yield in maize

High tolerance to salinity and osmotic stress, hormone modulation, nitrogen fixation, siderophore production, and phosphate solubilization in rice

Effect on plant

Brígido et al. (2019)

Zhang et al. (2018)

Walitang et al. (2017)

References

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disease severity caused by Verticillium dahliae by more than 30%. In hydroponics, P. indica increased fresh fruit biomass of tomato, the numbers of fruits, and the dry matter content. Uninoculated Pisum sativum plants treated with the soluble phosphate (positive control) produced the highest quantity of biomass (total weight, root weight, and shoot weight) in comparison to uninoculated control plants grown in sand containing insoluble phosphate (Oteino et al. 2013). Thus, inoculation with bacterial strain L132 showed the highest whole plant dry weight, enhanced plant growth, increased root, and shoot dry weight as compared to uninoculated treatments. This suggested that these strains solubilize the insoluble phosphate compound by release of gluconic acid present in the sand medium resulting in plant growth promotion as compared to E. coli JM109 strain (negative control). Increased plant growth and phosphate uptake have been reported in many crop species as a result of the inoculation of PSB Pseudomonas sp. particularly in rice (Gusain et al. 2015), soybean (Fankem et al. 2015), and wheat (Babana and Antoun 2006). Demissie et al. (2013) stated that the inoculation of fababean (Vicia faba L.) with phosphate solubilizing Pseudomonas and Rhizobium isolates resulted in enhanced plant growth under soluble phosphate limiting conditions as compared to uninoculated plants. Inoculation with PSB to the plants produced gluconic acid in the rhizosphere, resulted in the release of soluble phosphate, which was subsequently assimilated by the plant. However, these endophytic bacteria are also known to express other plant growth promotion traits such as IAA production and ACC deaminase activity, which may also have contributed to the enhanced growth of the inoculated plants (Otieno et al. 2015). Inoculation of the phosphate solubilizing endophytic isolate CKAM showed a remarkable increase in seed germination, shoot length and root length, shoot dry weight, and root dry weight of tomato under net house condition (Mehta et al. 2014). When the endophytic isolate CKAM was inoculated/co-inoculated with E. adhaerens (native rhizobia) to V. radiata, it significantly increased root length, shoot length, a number of lateral roots and plant dry weight of mungbean plants in a small field trial (Pandya et al. 2015). Endophytic bacterial strains isolated from the medicinal plant Lonicera japonica showed growth-promoting activities in wheat (Zhao et al. 2015). The inoculation of phosphate solubilizing endophytic fungi C. geniculata significantly promoted the growth of pigeon pea without expressing any pathogenic symptoms (Priyadharsini and Muthukumar 2017). Similarly, co-inoculation of endophytic diazotrophs and actinobacteria, i.e., Bacillus, Enterobacter, Microbispora, and Streptomyces significantly increased the growth parameters of sugarcane plants as compared to individual inoculation and uninoculated plants (Kruasuwan and Thamchaipenet 2016). Nitrogen-fixing endophytic bacteria P. stutzeri A15 from the rhizosphere of rice stimulated its growth (Pham et al. 2017). The endophytic bacterial strains isolated from rice seeds, i.e., Micrococcus yunnanensis RWL-2, Micrococcus luteus RWL-3, Enterobacter soli strain RWL-4, Leclercia adecarboxylata RWL5, Pantoea dispersa RWL-6, and Staphylococcus epidermidis RWL-7 produced a significant amount of IAA and such bacterial inoculation increased shoot and root length, fresh and dry biomass, and chlorophyll content of rice plants significantly (Shahzad et al. 2017). Inoculation of P. stutzeri strain E25 and Stenotrophomonas

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maltophilia strain CR71, which produced antifungal volatile compound dimethyl disulfide, promoted the shoot and root length, chlorophyll content, and total fresh weight of tomato plants (Lycopersicon esculentum cv Saladette) and their coinoculation further improved the plant growth-promoting effect (Rojas-Solis et al. 2018). Schmidt et al. (2018) reported that several endophytes including pseudomonads, Variovorax paradoxus, Verticillium leptobactrum, Halenospora sp., and Exophiala sp. enhanced growth of Miscanthus giganteus in gamma-sterilized soil in pot experiments. Moreover, co-inoculation of bacteria or fungi originating from Miscanthus promoted the growth of their host, especially on the heavy metals-polluted site. Similarly, inoculation of endophytic bacterium B. megaterium NMp082 isolated from root nodules of Medicago polymorpha promoted plant growth of Medicago lupulina, Medicago truncatula, and Medicago sativa. The co-inoculation of B. megaterium NMp082 with E. medicae further enhanced the growth and nodulation of Medicago spp. plants compared with inoculation with either bacterium alone (Chinnaswamy et al. 2018). Intrestingly, B. megaterium NMp082 also induced tolerance to salt stress in alfalfa and Arabidopsis plants due to salt stress alleviation effects. Pirhadi et al. (2018) reported that inoculation of bacterial endophyte Pseudomonas sp. SugS_49 isolated from sugarcane grown in saline soils showed more phosphorus dissolution ability and its inoculation increased the growth, grain yield, and phosphorus uptake of wheat. During the same year, Ribeiro and his colleagues reported that inoculation of Fe-P solubilizing endophytic Bacillus strains, produced high levels of IAA in the presence of tryptophan, enhanced the shoot and root dry weight, and the NPK content in plants cultivated in soil with no P fertilization (Ribeiro et al. 2018). Specifically, Bacillus strain B1923 enhanced shoot and root dry weight and root NP content of plants cultivated with no P added and Bacillus strains B2084 and B2088 showed positive performance on biomass production and accumulation of NPK in the shoot. Similarly, Kshetri et al. (2018) also reported that treatment with PSB obtained from the rhizosphere of Allium hookeri, resulted in enhanced growth of A. hookeri Thwaites. K. quasipneumoniae strain S6C2 increased root length and weight in TCP amended soil and increased available P in soil. Heydari et al. (2019) reported that under P deficiency, the dry root weight of barley significantly decreased the total root length with a decrease of root diameter under pot experiments. The results suggested that the root structure and root extension are directly and indirectly affected by soil fertility and especially P nutrient of the soil, which further determines plant growth and crop production. Sun et al. (2019) explored the beneficial effects of IAA-producing endophytic Pseudomonas poae strain S61 on medicinal plant Astragalus mongholicus. The combination trial also increased calycosin-7-O-glucoside and ononin accumulations in the roots, suggesting that the strain executed beneficial effects on A. mongholicus only when it grew under drought stress.

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3.8 The Genetics Involved in Endophytic Behavior and Phosphate Solubilization The genomic analysis could help to understand the mechanisms involved in decisionmaking regarding the influence of bacteria to act as endophyte because the capacity to penetrate and survive inside plant tissues are multifactorial. Moreover, rhizospheric bacteria colonize tissues inside plants, so that both lifestyles share a variety of mechanisms. In addition to testing of individual biochemical/genetic mechanisms involved in the interaction of a bacterial endophyte with a plant, it is possible to use a bioinformatics approach to predict some of the key features that distinguish endophyte from rhizospheric PGPB (Ali et al. 2014). The genomic DNA sequences of rhizospheric and endophytic PGPB (both Burkholderia spp.) were compared and the genes encoded by the rhizospheric strain were subtracted from the endophytic strain. Then, the remaining, putative endophytic genes, were compared with the complete genomes of eight different endophytic PGPB (B. phytofirmans PsJN, Burkholderia spp. strain JK006, A. lipoferum 4B, E. cloacae ENHKU01, K. pneumoniae 342, P. putida W619, Enterobacter spp. 638, Azoarcus spp. BH72, and S. proteamaculans 568). Genes that were common to all of these strains were considered to be potentially involved in endophytic behavior, including genes encoding transporter proteins, secretion and delivery systems, plant polymer degradation or modification, transcriptional regulation, detoxification, redox potential maintenance, unknown functions, and functions like 2-isopropylmalate synthase and diaminopimelate decarboxylase. Most of the (~40) genes identified by this procedure encode functions previously suggested by separate biochemical/genetic studies involved in endophytic behavior. Most of the genetic studies have been carried out on B. phytofirmans strain PsJN, a model endophytic bacterium, with the ability to competently colonize (both rhizosphere and endosphere) and promote the growth of a variety of different plant hosts, including A. thaliana, grape, maize, potato, switchgrass, tomato, and wheat (Sessitsch et al. 2005; Sheibani-Tezerji et al. 2015). Moreover, strain PsJN also increases tolerance of host plants to abiotic stress such as chilling and drought (Barka et al. 2006, Naveed et al. 2014), and biotic stress like inhibition of fungal phytopathogens (Sharma and Nowak 1998; Barka et al. 2006). Strain PsJN has been shown to require IAA degradation, ACC deaminase, and quorum sensing to colonize host plants and produce beneficial effects (Sun et al. 2009; Zuniga et al. 2013). Moreover, in planta gene expression profiling revealed that, during its growth inside host plants, the bacterium expresses several different traits related to cellular homeostasis, cell redox homeostasis, energy production, general metabolism (amino acids, lipids, nucleotides, sugars), and transcription regulation (Sheibani-Tezerji et al. 2015). The nitrogen-fixing endophyte Azocarus sp. was reported to infect plants through the emergence points of lateral roots and root tips via the action of bacterial endoglucanase (Rheinhold-Hurek et al. 2006). Also, transposon mutants lacking the activity of this endoglucanase colonized rice plants to a significantly lesser extent. This group subsequently showed that deletion mutants of the pilT and pilA genes in this

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bacterium abolished bacterial twitching and motility as well as the endophytic colonization of the roots of rice plants (Bohm et al. 2007), where pilT and pilA genes encode the pilus retraction protein and the pilin structural protein, respectively. On the other hand, the colonization of host plants by bacterial endophytes, showed that the gumD gene from the nitrogen-fixing endophyte G. diazotrophicus, involved in exopolysaccharide biosynthesis, is required for biofilm formation and subsequent root colonization (Meneses et al. 2011). It was later demonstrated the significance of endophyte colonization in rice plants of the gor and sod genes, a glutathione reductase, and a superoxide dismutase, analyzed in the N2 -fixing strain G. diazotrophicus (Alquéres et al. 2013). A series of DNA cytosine methylation changes were observed as a consequence of plant inoculation with the endophytic PGPB B. phytofirmans PsJN (Da et al. 2012). In this study, 30 plant proteins (thought to be involved in growth and signaling) and their methylation status was significantly altered (increased or decreased) and identified following interaction with the bacterium. When the effect of the endophytic PGPB G. diazotrophicus on sugarcane plants was assessed, using the proteomics approach of the more than 400 proteins that were analyzed, 78 were differentially expressed in the presence of the bacterium (Lery et al. 2011). To improve phosphate-dissolving capacity by PGPB strains, genetic transfer of any isolated gene involved in mineral phosphate solubilization (MPS) is an interesting approach. An attempt was made to improve MPS in PGPR strains, using a PQQ synthase gene from E. herbicola (Rodriguez et al. 2001). This gene was subcloned in a broad-host-range vector pKT230 and the recombinant plasmid was expressed in E. coli and subsequently transferred to PGPR strains of B. cepacia and P. aeruginosa. Several of the ex-conjugants that were recovered in the selection medium showed a larger clearing halo in medium with tricalcium phosphate as the sole P source. This indicated the heterologous expression of this gene in the recombinant strains and gave rise to improved MPS ability in these PGPRs. However, expression of the mineral phosphate solubilizing (mps) genes in a different host may also be influenced by the genetic background of the recipient strain, the copy number of the indigenous plasmids, and metabolic interactions. Mineral P solubilization involves the synthesis of gluconic acid, which is produced from glucose involving glucose dehydrogenase (GDH) enzyme (Goldstein and Liu 1987). The cofactor pyrroloquinoline quinone (PQQ) is required for GDH activity (Goldstein 1995). In pqq operon, pqqA, pqqB, pqqC, pqqD, and pqqE genes are conserved and arranged in an orderly manner, whereas, pqqF and pqqG are located either proximal or distal to the pqq operon (Shen et al. 2012). Moreover, a twocomponent regulatory system, consisting of a DNA-binding transcriptional regulator (PhoB) and transmembrane histidine kinase (PhoR) involved in regulation and secretion of various enzymes such as alkaline phosphatases, acid phosphatases, phytases, and phosphodiesterase in response to inorganic phosphate (Pi) scarcity (Santos-Beneit 2015). The alkaline phosphatase enzyme (encoded by gene phoA) of E. coli was fully induced when the Pi concentration was reduced from 100 mM to 0.16 mM (Lopez-Bucio et al. 2003), suggesting that a regulatory element called as Pi transport operon and the sensor-activator operon, both are involved in this mechanism. The genes controlled by Pi and activated by PhoB constituted the PHO

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regulon (Sashidhar and Podile 2009). The overexpression of phosphate uptake ABC transporter permease protein (PhoT) and the phosphate uptake ABC transporter ATP binding protein (phoC) in S. meliloti was found to enhance phosphate solubilization and yield in Medicago (Carmen and Roberto 2010).

3.9 Conclusion Plant beneficial endophytic microbes have great potential to act as biofertilizers and biopesticides for growth enhancement and protection from plant disease, respectively. Many bacterial endophytes can solubilize phosphorus, potassium, metals, and other toxic substances by producing various organic acids and enzymes. Moreover, the complex interactions in the rhizosphere and endophytic PSB with, other microorganisms, plant, and the environment-influenced solubilization of bound phosphates, Pi uptake, and plant growth promotion. Under field conditions, plant genotypes have been found as an important determinant in the development of a positive plantendophyte association. Majority of them containing endophytes tend to survive the harshness of the environment and challenge biotic and abiotic stresses. Altough, inconsistency in the performance of these inoculant strains is a major constraint to the widespread use of microbial inoculants in commercial agriculture (Rodriguez et al. 2006). It is, therefore, identification of the rare and promising bacterial endophytes with general plant beneficial characteristics would require a combination of culture-dependent and culture-independent techniques. With a further understanding of the functioning of bacterial endophytes, in the future scientists may be able to engineer bacterial endophytes to facilitate their potential to improve plant growth and development (Miller et al. 2010). The knowledge generated on biodiversity and genetic manipulation of P solubilizing endophytic bacteria thus require to design strategies for their efficient potential for sustainable and organic agriculture. This includes ecological consideration of single/group of microbial communities, their interactions in the rhizosphere or within roots (endophytes), their ability to mobilize P from different soil fractions, and farm management practices that influence these processes. More problems are yet to be resolved so as to utilize them in product development of biotechnological significance. The manipulation of bacterial traits with improved efficiency of P solubilization in endophytic bacteria and their inoculation as phosphatic biofertilizers may boost plant growth leading to improved soil health and crop productivity.

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Zhang Y, Kang X, Liu H, Liu Y, Li Y, Yu X, Zhao K, Gu Y, Xu K, Chen C, Chen Q (2018) Endophytes isolated from ginger rhizome exhibit growth promoting potential for Zea mays. Arch Agron Soil Sci 64(9):1302–1314 Zhao L, Xu Y, Lai XH, Shan C, Deng Z, Ji Y (2015) Screening and characterization of endophytic Bacillus and Paenibacillus strains from medicinal plant Lonicera japonica for use as potential plant growth promoters. Brazilian J Microbiol 46(4):977–989 Zhao S, Wei H, Lin CY, Zeng Y, Tucker MP, Himmel ME, Ding SY (2016) Burkholderia phytofirmans inoculation-induced changes on the shoot cell anatomy and iron accumulation reveal novel components of Arabidopsis-endophyte interaction that can benefit downstream biomass deconstruction. Front Plant Sci 7:24–35 Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P, Ishimaru CA, Arunakumari A, Barletta RG, Vidaver AK (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microbiol 68:2198–2208 Zuniga A, Poupin MJ, Donoso R, Ledger T, Guiliani N, Gutierrez RA, González B (2013) Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol Plant-Microbe Interact 26:546–553

Chapter 4

Cattle Dung Manure Microbiota as a Substitute for Mineral Nutrients and Growth Management Practices in Plants Sandhya Dhiman, Sandeep Kumar, Nitin Baliyan, Shrivardhan Dheeman, and Dinesh Kumar Maheshwari Abstract Minerals are ubiquitous and found in two forms “macronutrients and micronutrients” in soil. To meet out their requirements to crops. Cow dung is high in organic materials rich in nutrients and contains (3-2-1 NPK) besides rich in ammonia. On the other hand, dung and manure is the source of potentially beneficial bacteria used as a rich fertilizer and produce biogas which is eco-friendly and an alternative to fossil fuels. Cow dung has been used in various forms for centuries, like fires, for heating, cooking. Hindu rituals performed during popular festivals. A diverse group of microbes inhabiting in dung mainly bacteria has multiple roles such as plant growth promotion and protection from diseases in plants. The addition of dung corroborates nutrients, micronutrients, and organic matter availability to soil and favors growth/activity of symbiotic bacteria resulting in improved biomass. Composting for agricultural benefits is the need of today to help in the reclamation of degraded soil of wastelands. The application of dung/compost and microorganisms act as catalysis for farmers in developing countries to exploit microbiota for augmenting the crop productivity, and ensuring continued maintenance and building up of the soil fertility for greater sustainability. Keywords Dung · Nutrients · Microorganisms · Soil fertility · Plants

S. Dhiman (B) · S. Kumar · N. Baliyan · S. Dheeman · D. K. Maheshwari Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India e-mail: [email protected] S. Dheeman e-mail: [email protected] S. Dheeman Department of Microbiology, School of Life Sciences, Sardar Bhagwan Singh University, Dehradun 248 161, Uttarakhand, India © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_4

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4.1 Introduction Today’s challenge in modern agriculture is to attain high agrobiological sustainability in terms of crop productivity and soil health. Although during green revolution, the exhibited use of synthetic fertilizers accomplished crop’s high yield but at the same time also led to adverse effects such as degradation and acidification of soil, mismanaged ecology, deterioration of soil fertility, and decrease in the yield of the crop (Ju et al. 2009). The major goal of nutrient management is to enhance agronomic crop productivity to meet the food demands of the ever-increasing population. The chemical fertilizers disturb the soil physiochemical properties viz., soil texture, porosity, water holding capacity, and beneficial soil microbial flora. The usage of inorganic fertilizers has drastically dropped due to the energy crisis, which has immensely affected most of the developing countries (Gulshan et al. 2013). A low-input agricultural system which relies on the input of organic materials holds great promise not only to diminish the use of synthetic fertilizer but also to recover crop productivity and ensure ecosystem sustainability against nutrient mining and degradation of soil and water resources (Tilman et al. 2002; Kravchenko et al. 2017). Soil is a sink of plant nutrients that remain in both soluble and insoluble forms. Plants can easily take up the former but difficult to get assessed with insoluble forms which are transformed into a soluble form by various mechanisms (Maathuis and Diatloff 2013). A large group of diverse microbiota inhabiting in the soil transform insoluble minerals into accessible form for their uptake by plants. Microbial activity is essential for the release of nutrients from dung without such release the available plant nutrient supply would soon be hampered and the soil would become infertile (Jin et al. 2016). Microbes inhabiting in dung complete the cycle by returning into the soil those nutrients the plants’ uptake from it (Chen et al. 2015). An active, thriving microbial population is a good bio-indicator of fertile soil. The shortage of fuelwood is a major problem hence, forces the rural people to use the dung for their fuel purpose, which affects the productivity status of cultivated land. In India tons of the livestock dung produced annually, it remains unutilized or is not being fully utilized results in a loss of buffalo dung 12.20 kg dung in a day and cow dung 11.6 kg animal/day and goat dung 0.70 kg animal in a day (Chauhan and Singh 2012). Further, livestock waste acted as the chief source of noxious gases (greenhouse gas), pollution, pathogens, and odor having communal health and environmental pollution (Martinez et al. 2009) which adversely affect air quality especially in rural areas dung acts as cooking fuel coupled with poor ventilation (https://www.indiatimes.com/news/india/pollution-due-to-burningof-cow-dung-wood-as-fuel-killed-1-24-lakh-people-in-one-year-332719.html). The share of the Indian population relies on traditional biomass for cooking stands at 72%. Bekele et al. (2013), observed 943 metric tonnes of, dung used by households annually. As a result, N, P, K, Ca, Mg, and Fe nutrients are lost per year, This practice hurts the nutrient balance of the soil and consequently affects agricultural productivity. Investigators found that while the dung burnt in the kitchen contains as much as 25% of the arsenic in fumes (indoor) absorbed by the respiratory tract of people thus leads to diseases such as persistent cough and chronic

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bronchitis (https://www.downtoearth.org.in/news/cow-dung-smoke-could-cause-ars enic-poisoning–4002). Hence, its proper management is yet to be done to mitigate these pollutants to shield the environment from obnoxious gases. Air pollution (methane, CO2 , etc.) also contributes to greenhouse gases (GHGs) leading to climate change (Ramanathan and Feng 2009). Various workers reported management strategies to reduce the wastage of animal dung and minimize soil toxicity (Li et al. 2016a). The proper utilization of livestock waste into biogas (Afazeli et al. 2014), compost formation (Bernal et al. 2009), and vermicomposting (Garg et al. 2005) assisted to accomplish an increase in crop yield and sustainability (Chadwick et al. 2015). Likewise, utilization of them in terms of organic fertilizers provides an opportunity for the agricultural sector for organic farming thus, lessen their reliance on chemical fertilizer (Bandyopadhyay et al. 2010). Dung is a mixture of many mineral nutrients found to contain crude fiber, crude protein, cellulose, hemicellulose, and 24 types of minerals such as nitrogen, potassium, along with trace amount of sulfur, iron, magnesium, copper, cobalt, manganese, etc. Generally, dung contains approximately 80% water and matrix of undigested plant material, rich in nutrients, microorganisms, and their by-products. Whereas, indigenous Indian cow comprises a higher sum of calcium, phosphorus, zinc, and copper than the other minerals (Garg and Mudgal 2007; Randhawa and Kullar 2011). Therefore, the nutrient management of dung is essential to enhance agronomic productivity (Gholamhoseini et al. 2013). Animals play an important role in energy generation processes such as by converting plant energy into useful work, e.g. dung used for fuel through dung cakes and biogas to replace for soil fuel, i.e. charcoal, fuelwood, firewood, etc. (Raj et al. 2014). Available literature revealed that dung acts as a disinfectant for the home in a rural area and now available in the form of wood used for fuel purposes.

4.2 Microbiology of Dung Although, animal dung has been extensively exploited for its use as organic agricultural fertilizers, as well as alternative fuel/biogas due to high methane content (Abdulkareem 2005). But research on the microbial diversity and other potential applications of cattle dung (Gattinger et al. 2007) is yet to be established (Yokoyama et al. 2007; Dhiman et al. 2019). Microbial flora of dung includes both aerobic and anaerobic microorganisms including an abundant number of bacilli, lactobacilli, cocci, and some identified and unidentified fungi and yeasts (Muhammad and Amusa 2003; Vijayaraghavan et al. 2006; Swain et al. 2012). Various bacterial genera viz., Citrobacter koseri, Enterobacter aerogenes, Escherichia coli, Klebsiella oxytoca, Klebsiella pneumoniae, Kluyvera spp, Morgarella morganii, Pasteurella spp, Providencia alcaligenes, Providencia stuartii, and Pseudomonas spp. have been reported from cow dung (Sawant et al. 2007). In addition, the lower part of animal gut includes Lactobacillus plantarum, Lactobacillus casei, Lactobacillus acidophilus, Bacillus subtilis, Enterococcus

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diacetylactis, Bifidobacterium spp. and yeasts (commonly Saccharomyces cerevisiae), possessing probiotic activity (Ware Fungsin et al. 1988). Dung inhabiting methanogens particularly Archaea and the phylum Euryarchaeota including Methanomicrobium, Methanobrevibacter ruminantium, Methanobacterium formicicum, Methanomicrobium mobile, Methanosarcina barkeri, etc., are not only confined to the rumen in cattle and other ruminants but proved an excellent source of bioenergy. Swain and Ray (2009) studied that B. subtilis isolated from cow dung enhanced plant growth, phosphorous solubilization, sulfur oxidation and was found to yield industrial products. Their presence has now been discovered in the soil since dung is has been accepted as a soil fertilizer since pre-historic time (Hook et al. 2010). Recently, cow dung has been proved an excellent source of the management of soil nutrients (Dhiman et al. 2020). Few of them are listed in Table 4.1. Table 4.1 Diversity and distribution of microorganisms in cattle dung Microbial strains

References

Bacillus cereus, Bacillus Subtilis

Muhammad and Amusa (2003)

Paenibacillus favisporus

Velazquez et al. (2004)

Bacillus subtilis

Swain et al. (2012)

B. pumilus, B. macereans, B. sphearicus, B. laterosporus, Micrococcus varians, Proteus mirabilis, E. aerogens

Adegunloye et al. (2007)

Pseudomonas spp., Bacillus spp.

Akinde and Obire (2008)

Enterobacter spp., Rahnella spp.

Fuentes et al. (2009)

Citrobacter spp.

Pandey et al. (2009)

Pseudomonas jessenii, P. synxantha

Srivastava et al. (2010)

Thermoanaerobacterium thermostercus

Romano et al. (2010)

Ruminococcus sp., Enterococcus casseliflavus/gallinarum

Wahyudi et al. (2010)

Bacillus sp.

Teo and Teoh (2011)

Clostridium cellulosi

Carillo et al. (2012)

Bacteroides, Fermicutes, Proteobacteria

Girija et al. (2013)

Lysinibacillus xylanilyticus, B. licheniformis, B. subtilis, B. cereus

Radha and Rao (2014)

Pseudomonas xanthomarina, P. stutzeri, and Bacillus niacin Das et al. (2017) Pseudomonas otitidis, Stenotrophomonas korensis, Serratia marcescens

Vyas and Kumar (2018)

Bacillus cereus

Croos et al. (2019)

Proteus mirabilis

Dhiman et al. (2019)

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4.3 Dung: Bioresource of Energy At present, the consciousness of organic matter and the concept of sustainable agriculture have been achieving impetus among Indian farmers to produce good quality consumable agricultural products (Eastman et al. 2001). Natural resources to generate energy always proved to be an important issue in the enhancement of the economy of India. In this context animal waste can be cost-effectively used to produce energy while contributing a significant portion of energy independence, and reducing disposal costs and pollution (Kemausuor et al. 2016). As stated earlier, the availability of animal dung is produced in large quantities, thus forms a sound base for nonconventional energy. Chynoweth et al. (1993) suggested as potential sources of biogas production include cattle waste, buffalo waste, piggery waste, chicken waste including human excreta. Due to an abundance of dung availability and rich in organic matter, it is easily accessible for biogas production and acts as a rich habitat for various microbes such as methanogens, hydrogen-producing, and cellulose-degrading bacteria. In India, methane is popularly called “gobar gas” and produced by anaerobic microorganisms. The scientists engaged this work stated that organisms work synergistically that it can do more than is estimated by “summing.” Although, a large number of facultative anaerobic or obligate anaerobes have been involved in various microbial reactions for energy (biogas) generation processes the exact role of individual organism is yet to be determined (Güllert et al. 2016). Some of the microorganisms involved in synthesizing various products given in Table 4.2. A diverse group of bacteria such as Pseudomonas sp., Azotobacter sp., and other purple sulfur or purple non-sulfur bacteria is the main inhabitants of dung responsible for the production of the maximum amount of methane gas in comparison to other photosynthetic bacteria (Zhao et al. 2013). The anaerobic fermentation of animal wastes does not require the addition of seed bacteria for biogas production, and this feature differentiates animal waste from other organic wastes (Yokoyama et al. 2007). The animal waste on this planet produces around 55–65% methane, which upon release in the atmosphere can affect global warming 21 times higher than the rate CO2 does (Abbasi et al. 2012). Methanogens, a dominant heterogeneous group of and/or bacteria/archaea ferment organic matter of the dung anaerobically produce biogas which is a mixture of different gases mainly constitutes methane (50–65%) and CO2 (25–45%). Dung excreted by 3–5 cattle/day can run a biogas plant of 8–10 m3 which can yield 1.5– 2 m3 biogas per day, enough for the family of 6–8 persons, can cook a meal for 2 or 3 times or may light two lamps for 3 h or run a refrigerator for all day and can also operate a 3-KW motor-generator for 1 h (Stanley et al. 2013). Earlier, Ranade et al. (1990) analyzed the effect of different total solid contents on biogas production and reported that the optimum production occurred at 8%. Interestingly, Garg et al. (2005) reported that buffalo dung contained 22.3% solid contents. A 1-m3 biogas plant produced 28.78 l/kg (0.028 m3 ) to 32.76 l/kg (0.032 m3 ) of biogas, respectively, when daily feed with 22 kg of dung/m3 which is mixed with an equal amount of water

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Table 4.2 Methanogenic bacteria and products formed from their respective substrates Bacterium

Substrate

Products

Methanobacterium formicum

CO H2 + CO2 Formate

CH4

M. mobilis

H2 + CO2 Formate

CH4

M. propionicum

Propionate

CO2 + acetate

M. ruminaticum

Formate H2 + CO2

CH4

M. soehngenii

Acetate butyrate

CH4 + CO2

M. suboxydans

Caproate and butyrate

Propionate & Acetate

Methanococcus mazei

Acetate and butyrate

CH4 + CO2

M. vannielli

H2 + CO2 Formate

CH4

Methanosarcina barkerii

H2 + CO2 Methanol acetate

CH4 CH4 CH4 + CO2

M. methanica

Acetate butyrate

CH4 + CO2

Source Chawla OP (1986) Advances in biogas technology

with 9–10% of total solids. The maximum production of biogas from that plant is 39.00 l/kg (0.039 m3 ) and 40.04 l/kg (0.04 m3 ), respectively, when operated at the temperature of 23.5 °C (Carotenuto et al. 2016). On the other hand, the farmers also obtain 13.87 metric tons of organic fertilizer per year from the biogas plant. Romano et al. (2010) investigated the suitability of buffalo manure bacterial community for biogas production. Stimulation of biogas production from dung mixing with cattle urine reported four times in comparison to dung alone. Cattle urine dung-slurry gives increased biogas production (Mutesasira et al. 2015). Studies suggested that the microbial populations in dung come from endophytic bacteria of fodder grasses. It has been established by workers that some of the bacteria have the ability of colonization in interior tissues of a host plant and form a beneficial symbiotic association to improve the growth of the host plant (Li et al. 2016b). Sphingomonas, Bacillus, Pantoea, Enterobacter, Pseudomonas, etc., are some of the reported endophytes in fodder grasses. Other than these, few more endophytes have also been reported as given in host in Table 4.3.

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Table 4.3 Endophytic bacteria associated with animal feed Source

Genera

References

Zoysia japonica

Acremonium endophytes

Zhibiao (1996)

Vitis vinifera, Panicum virgatum

Burkholderia phytofirmans, Burkholderia sp.

Compant et al. (2010)

Melinis minutiflora

Azospirillum melinis

Peng et al. (2006)

Zea mays kernels

Pantoea sp., Frigoribacterium sp.,

Rijavec et al. (2007)

Brachiaria decumbens

Bradyrhizobium sp.

Kelemu et al. (2011)

Medicago sativa

Micromonospora sp.

Martínez-Hidalgo et al. (2014)

Deschampsia flexuosa

Pedobacter sp., Enterobacter sp.a , Xanthomonas sp., Paracoccus sp.

Poosakkannu et al. (2015)

Pennisetum purpureum, Medicago sativa

Sphingomonas paucimobilis, Bacillus megateriuma

Li et al. (2016a), Stajkovi´c et al. (2009)

Cymbopogon citratus

Bacillus spp.a , Escherichia colia , Klebsiella pnuemoniae, Micrococcus spp.a , Pseudomonas sppa .

Inuwa et al. (2017)

Beta vulgaris, Phragmites australis

Pseudomonas sp.a , Xanthomonadale sp. Piernik et al. (2017), White et al. (2018)

Leersia oryzoides

Microbacterium sp., Pseudomonas baetica, Pantoea hericii, Paenibacillus sp.a , Pseudomonas oryzihabitans, Pantoea vagans

a Dung

Verma et al. (2018)

inhabitants

4.4 Dung: Source of Industrial Products By advantage of the microbial inhabitants bacteria and other microorganisms of extremophilic nature, scientists took advantage of the microbiota for industrial applications. The bacteria or their metabolites are extraordinary and play an important role in nature and at industrial level. Such as they secrete stable enzymes at extreme temperature and pressure, can be used for biodegradation and bioremediation, can be a good source of biofuel and bioenergy. These are the source of specialized pigments for solar cells able to work in extreme conditions such as polar caps (Arora and Panosyan 2019). There is a non-stop search for the plausible microorganisms that are in a position to synthesize industrially viable chemicals of biotechnological importance. The range of microbes in cow dung makes an attainable supply for the discovery of novel major and secondary metabolites (Meena et al. 2013). Bacillus spp. inhabiting in cow dung can produce cellulases, pectinases, and hydrogenases, etc. (Singh et al. 2013; Vijayaraghavan et al. 2016). Novel thermotolerant endoglucanase (CMCase) has been purified and characterized from Bacillus strain inhabiting in cow dung (Sadhu et al. 2013). Few thermotolerant bacteria with the capability of producing thermotolerant enzymes like protease, lipase, and esterase

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Table 4.4 Organic acids secreted by bacteria isolated from dung Bacteria

pH

Temperature (°C)

Acids formed

Bacillus cereus

5.2

25–30

Acetic, lactic

Bacillus knelfelkamipi

5.2–8.0

25–35

Acetic, lactic

Bacillus megaterium

5.2–7.5

28–35

Acetic, lactic

Bacteroides succinogenes

5.2–7.5

25–35

Acetic, succinic

Clostridium carnofoetidum

5.0–8.5

25–37

–

Clostridium cellobioparus

5.0–8.5

36–38

Formic, acetic, lactic, ethanol, CO2

Clostridium dissolvens

5.0–8.5

35–51

Formic, acetic, lactic, succinic

Clostridium theymocellulaseum

5.0–8.5

55–65

Formic, acetic, lactic, succinic, ethanol

Pseudomonas formicans

–

33–42

Formic, acetic, lactic, succinic, ethanol

Ruminococcus flavifaciens

–

33–38

Formic, acetic, succinic

Source Chawla OP (1986) Advances in biogas technology

lipase have been detected in manure compost (Charbonneau et al. 2012). Previously, xylanolytic bacteria have obtained growing industrial activity in numerous industries such as enzyme-aided bleaching of paper (Velazquez et al. 2004), production of ethanol from plant biomass, animal feed additives). A member of xylanolytic bacteria Paenibacillus favisporus sp., from cow dung, produced an extensive range of hydrolytic enzymes such as xylanases, cellulases, amylases, gelatinase, urease, and β-galactosidase (Velazquez et al. 2004) showed feasible for industrial applications. The occurrence of naturally occuring steroid hormones in dung has also been reported by several workers (Ermawati et al. 2007; Andaluri et al. 2012). Mohanta et al. (2017) reported Bacillus sp. as amino acid-producing bacteria from cow dung and amino acids namely cysteine, serine, and methionine were characterized by Bacillus sp. These amino acids are the building blocks of proteins, constitute a major part of the body, involved in building cells and repairing tissues, and form antibodies to combat foreign bodies like bacteria and viruses. Longback, Chawla (1986) mentioned both strong and weak organic acids, ethanol, and other metabolites are produced by a different group of bacteria as given in Table 4.4.

4.5 Dung and the Mineral Nutrients Management The interest in the use of dung has increased exponentially especially to preserve soil fertility for the long term. Dung contains small portions of plant nutrients in inorganic forms that do not require mineralization to be solubilized in the soil water solution. This solubilized fraction has a direct influence; its nutrients are easily available for plant uptake, while the organic forms of plant nutrients in dung provide the slow

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release effect for nutrients through the growing season, given the reason for suitability for environmental and soil conditions because of the gradual release of plant nutrients (Eghball et al. 2002). It is yet to consider a match between nutrient release from dung and plant demand for nutrients; mismatch might result in nutrient leaching (main nitrate in humid areas), toxicity, or nutrient deficiency. Nevertheless, sole compost is not enough to satisfy the farm production to cover the whole nutrients requirements in a short-term period. Besides, meeting crop demand for nutrients through organic matter supply does not guarantee optimum supply of minerals require for crop yield due to the fact that the decomposition of organic matter is a climate-dependent process (Wall et al. 2008). On the other hand, organic matter amendments in soil stimulate the biological activity, which makes the nutrients cycle less predictable (Tao et al. 2015). Therefore, organic farming practices include rotation of legume crops, green manuring, returning uncomposted agricultural wastes to soil, and crop residues incorporation in the fertilization schemes assist to provide, soluble fractions of the essential nutrients (Reckling et al. 2016). Incorporation of green manure crops into soil provides a considerable amount of soluble nutrients into the soil system. Ewulo et al. (2007) observed the comparative effect of cow dung manure on soil and leaf nutrient and yield of pepper. The nutrient analysis in different manure is given in Table 4.5. Since historic times in India, cattle dung is accepted and utilized in many ways. The potential of dung in enhancing soil fertility was known to Indian sub-continental farmers for centuries, but little was known regarding role of dung microorganisms in mediating nutrients cycling in soil (Nopparat et al. 2007). Various workers have reported that these microorganisms play a significant role in composting by the decomposing organic substrate (aerobically) into carbon dioxide, water, minerals, and stabilized organic matter (Bernal et al. 2009; Kala et al. 2009; Vakili et al. 2015). Current literature revealed that researches related to the isolation and characterization of the beneficial bacteria present in biodynamic preparations are few (Giannattasio et al. 2013). A definitive proof is required to know whether bacteria in such formulations have plant growth-promoting rhizobacteria (PGPR) attributes and can improve Table 4.5 Average nutrient content of bio-compost of animal’s origin

Manure type

Nutrient content (%) N

P

K

Cow

0.30–0.45 0.15–0.25 0.05–0.15

Buffalo

0.5–0.9

0.21–0.3

0.05–0.17

Chicken

3.15

1.64

2.07

Poultry manure

2.87

2.93

2.35

Cattle waste vermicompost 0.51–1.61 0.19–1.02 0.15–0.73 Vermicompost

1.20

0.004

0.37

Farm yard manure

0.80

0.41

0.74

Source Miner JR, Smith RJ (1975) Livestock waste management with pollution control

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plant growth under defined conditions in soil microcosms, that overcome the drawbacks of field experiments by eliminating the errors arising from spatial variability of soil physicochemical and fertility properties occur in field gradients (Kalita et al. 2015).

4.6 Dung on Nutrient Uptake in Plants Nowadays, quality not the quantity of crop considered its merit from a commercial marketing point of view. This is the reason organic fertilizers raised crops have been fetching good markets and presently being used as a common agricultural best practices (Ahmad et al. 2019). Moreover, from awareness of the health consciousness point of view consumers are more interested in food of good nutritional quality having devoid of chemical residues in the edible part of the plant. The production of such organic products accomplished due to environmentally friendly and sustainable agricultural practices from economic point of view (Roberts and Mattoo 2018). Amendment of dung increases pH, total nitrogen, and organic carbon, loss on ignition, and exchangeable magnesium and calcium and decreased sulfate sorption in soil (Raj et al. 2014). The dung manure played a noteworthy role in maintaining the nutrient status of the plant (Sukartono et al. 2011). Nevertheless, nutrients contained in animal manures are released more slowly and are stored for a longer time in the soil ensuring longer residual effects similar to the long-term effect of some beneficial plant growth and health supporting bacteria (Maheshwari 2011) on growth and development of crops (Sharma and Mittra 1991; Abou El-Magd et al. 2005). Animals excrete N (nitrogen), phosphorus (P), and potassium (K) in the ingested feed, and these elements also appear in the manures. Thus, manure composition depends on the quality of the animal feed offered to the animals; feeds high in protein would give high nitrogen manures. The more phosphorous and potassium are in the feed, the richer is the manure of these nutrients (Ghosh et al. 2004). Hence it would be a noteworthy and eco-friendly farm practice, besides improving soil fertility by activating soil mineral status and microbial biomass (Ayuso et al. 1996). The manure nourishes soil organisms which gradually provide nutrients accessible to plants. Manures have dual role (i) it contains all necessary nutrients in available forms and (ii) improve the physical and biological properties of the soil (Abou ElMagd et al. 2006). Murmu et al. (2013) observed that organic manure increased crop productivity, nitrogen utilization efficiency, and soil health in tomatoes (Lycopersicon esculentum) and corn (Zea mays) in acidic soil and if animal manures applied optimally an outstanding effect on the growth and yield of crops remains visible (Makinde and Ayoola 2008). Manures withstand cropping system through improved nutrient recycling (Powell et al. 2002). Goat dung manure also exhibited significant influence on nutrient availability in soil, nutrient status, depicted as an effective source of N, P, K, Ca, Mg, and organic matter for promotion of healthy pepper production. Samuel et al. (2003), observed in pepper crop productivity (Awodun et al. 2007), improved yield of

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okra, amaranthus, celosia, and maize (Odiete et al. 1999; Ojeniyi and Adegboyeaga 2003a) by adding organic manure. Kaur et al. (2005) also reported that organic manure increased the soil of organic C, N, P, and K, thus highlighting its importance in tropical farmland. Poultry manure, a good source of organic matter, played a vigorous role in soil fertility enhancement, as well as furnishing micronutrients for crop production. Earlier, Amiri, and Fallahi (2009) observed that the application of poultry manure improved the availability of the mineral in soil, hence assisted to facilitate nutrient uptake in the plant. Nowadays improper utilized poultry waste becomes a foremost problem, thereby polluting the environment. Since poultry farm holders use concentrates for feeding as a result of which the excreta cannot be used as fuel, except as a good source of manure in the crop fields (Zake et al. 2010). Olasekan (2018), observed the effect of poultry manure on soil properties, growth and fruit yield of tomato. Adekiya et al. (2019) reported the effect of poultry manure to improved soil physical and chemical properties, leaf nutrient concentrations, and yield components of radish.

4.7 Dung Applications: Success and Bottleneck It reminds us of an era of the late 1960s that was the food security for the everincreasing population, particularly in India. Scientists started using agrochemicals for productivity enhancement of some major crops such as wheat and rice. Later, it was realized that the application of chemical fertilizers not only injurious to humans but also have adverse consequences on the soil water ecosystem. Soil productivity maintenance is a major constraint of the tropical agriculture system. Low soil fertility was one of the greatest biophysical constraints to the production of crops across the world (Ajayi 2007). Tropical soils are unfavorably affected by suboptimal soil fertility and erosion, instigating deterioration of the nutrient status, and changes in soil organism populations (Akande et al. 2010). Scientifically, soil amended with animal dung proved a very good source for sustaining crop production and increasing the beneficial microbial population in the soil (Raj et al. 2014). All animal origin wastes such as farmyard manure, poultry manure, and cattle/cow dung have dual advantages being cheap and contain nutrients that support healthier root development leading to higher crop yield (Abou El-Magd et al. 2005). Chemical fertilizers are costly and are not easily available to the majority of the smallholder farmers, particularly in hilly states of India having marginal farm income, hence compelled farmers toward the organic sources to substitute soil nutrients. Besides organic resources are frequently projected as an alternative to commercial chemical fertilizers. In this scenario, dung is easier and cheaper to transport, handling, and storage. It has multiple benefits due to the balanced supply of nutrients, including micronutrients, increased soil nutrient availability due to soil microbial activity. Such activities occur due to various biochemical reactions involved in soil respiration and another bioactivity. The alteration of pH, temperature resulted in a change in soil structure and function (Pettersson and Bååth 2003; Samuel et al. 2003) (Fig. 4.1).

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Fig. 4.1 Merits of dung over chemical fertilizers

The decomposition of harmful elements, soil structure improvements, root development, and increased soil water availability are added advantages (Zingore et al. 2008). On the other hand, chemical fertilizer reduces crop protein content, carbohydrate quality, etc., (Marzouk & Kassem 2011) while excess potassium content on chemically overfertilized soil quality further decreases several components of vegetable and crop (vitamin C, carotene content, and antioxidant compounds) as observed by Toor et al. (2006). Whereas, vegetables and fruits grown-up on overfertilized soils (chemically) are more disposed to insecticidal attacks and disease (Karungi et al. 2006) and crops become more vulnerable to abiotic stresses. Dungbased manures have a long-term impact on soil, maintaining fertility for a longer time (Table 4.6). Scientists also worked upon Physicochemical properties with special reference to dung properties such as total solid content, moisture content, dry matter content, etc. It was noticed that the total solids (TS) content in the dung obtained after the evaporation of water comprises neither too high nor too low (around 12%) as the concentration of TS contents affects the survival of microorganisms (Gunnerson and Stuckey 1986). Earlier, Garg et al. (2005) reported pH 8.4 in the case of buffalo dung whereas Murphy (2006) found that manure pH was typically neutral (7.0) to alkaline. Due to the fact, Schnurer and Jarvis (2010) stated and enumerated a maximum number

4 Cattle Dung Manure Microbiota as a Substitute … Table 4.6 Comparison of soil properties with addition of dung

Characteristics

89 Dung

Dung+Soil (1:3)

pH

5.1

6.5

OC (%)

37.1

40.2

N (ppm)

40.1

86.3

P (kg/ha)

121

135.3

K (g/kg)

0.276

0.997

Moisture (%)

68

71

Lab unpublished data. Values are mean of three replicates

of microorganisms prefer a neutral pH range 7.0–7.5 (Schnurer and Jarvis 2010). The optimum moisture content remained in the range of 60–95% (Demetriades 2008). Hollmann et al. (2008) examined the dung obtained from Holstein and Jersey cows produced 5.80 kg/d of total solids. Similarly, Wang et al. (2007) estimated that 16.7% dry matter content whereas Gautam et al. (2016) obtained the average dry matter percentage in cow and buffalo dung in the range of 38% and 14%, respectively. The manure or compost equally important for plant-soil-microbe interactions and is safe for health and environment. To achieve enhanced environmental conditions, advocating the use of organic materials is indispensable (Bayu et al. 2006). Studies revealed the significant effect of compost pig manure and cattle dung on the enhancement of yield and quality leafy vegetables like spinach, lettuce, and cabbage (Yamazaki and Roppongi 1998). Sharma and Bhalla (1995) also reported enhanced growth and yield in okra with the application of fermented dung and slurry. In the last decade, Jawale et al. (2009) obtained the highest yield and quality of spinach with use of dung, urine slurry followed by sheep, goat, and buffalo. The improper use of dung needs to be stopped and should only be applied in the farmland so that the productivity and sustainability of soil could be maintained for the production capacity of food treasure (Bhattacharyya et al. 2007). Various workers reported advantageous effects of organic manure on plant-soil properties (Adeleye et al. 2010), with reference to bulk density, water holding capacity, and other soil physical properties (Fawole et al. 2010). Effect of organic manure enhanced aeration, drainage, and friability of the soil (Schjønning et al. 1994; Maheswarappa et al. 1999; De Silva and Cook 2003). The organic matter of manure facilitates plants to use the nutrients for a long time, due to its slow decomposition and reduces the loss of what is not utilized by the plants (Bhandari et al. 2002). This property leads organic manure for sustained crop production through better nutrient recycling and improvement of soil physical attributes, environmental conditions, and public health (El-Shakweer et al. 1998; Ojeniyi 2000; Maritus and Vleic 2001). In fact, amendment of organic manures in soil attained maximum and sustainable crop yield, besides enhancing soil fertility and productivity (Sanwal et al. 2007). Due to abundance, cattle and swine manure have been extensively used in agricultural fields in India. The composted form of these manure proved better in comparison to that of fresh manure because it eradicates the risk of loss of nitrogen by

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leaching and surface runoff, suppress soil-borne pathogens, increase soil organic matter, and to mitigate greenhouse gas emissions (Darby et al. 2004; Evanylo et al. 2008; Escribano 2016). Mbah (2006) observed that poultry, cow dung, and swine manure increased uptake of K, Ca, and Mg in maize. The addition of cow dung in the soil enhances the physical and chemical properties of soil by increasing its fertility (by adding nutrients), moisture-absorbing capacity, etc. If used in clay soils where water logging is a problem cow dung increases the porosity of soil but if the soil is porous not retaining the water such as sandy soil, then cow dung acts as water holding carriers (Gbenou et al. 2017), increases the geotechnical properties like bulk density, dry density, porosity, infiltration (Ekwue et al. 2009). Cow dung is an important source of organic matter in soils, especially in small-scale farming systems across the globe. For degraded soil, the soil’s physical properties are usually destroyed, because the organic matter has declined in the soils. Thus, cow dung/organic has a significance in increasing the soils buffering capacity, to regulate soil acidity. This reduces soil aggregation and soil bulk density, water holding capacity, and nutrient holding capacity. The presence of organic matter ensures that soil biological properties are optimally functional in soil system. Increase the water holding capacity of soil corresponds to increase the growth of the plant and sustain productivity as stated by various workers (Zheng et al. 2018). Replacing chemical fertilizers with organic manure reduced the environmental pollution and also minimizes organic waste (Ram et al. 2007). Application of organic manure improves chlorophyll content in leaf and N, P, K, Fe, Zn, and Mn contents in olive trees (Abdel-Nasser and Harash 2001; Abou El-Khashab et al. 2005), and enhanced vegetative growth parameters of guava tree (Ram et al. 2007). In case of poultry manure, increased yield, quality production, and nutrient uptake were recorded in mustard (Zamil et al. 2004) and Foeniculum vulgare (Dhiman et al. 2019). Earlier, Sobulo and Babalola (1992) also studied the role of poultry dropping and cattle dung on the growth and enhancement of maize root growth. Continuous use of cattle manure increases crop yields with fertilizer phosphorus (Reddy et al. 2000). Ghosh et al. (2004) checked the comparative effect of cattle manure, poultry manure, phosphor-compost, and fertilizer-NPK on three cropping systems in vertisols of semi-arid tropics and concluded their significance on nutrient management in plants. Cattle manure has been recognized as an effective strategy to maintain an adequate supply of organic matter in the soil. It was also observed that animal manure improves the physical and chemical conditions of soil along with the enhancement in crop performance (Ikpe and Powell 2002; Powell et al. 1998). Various workers revealed the significance of poultry, cattle, goat, sheep, and pig manure to improve soil fertility and crop yield (Adeniyan and Ojeniyi 2003; Ojeniyi and Adegboyega 2003b). Nyakatawa et al. (2001) also reported that the application of organic manure increased yield of crops, besides maintaining soil fertility after adopting appropriate tillage practices. The addition of compost into the soil tends to improve nutrients and water holding capacity (Arslan et al. 2008; Vakili et al. 2015). Ewulo (2005) examined the relative effect of poultry and cattle dung on the chemical properties of soil. Adediran et al. (2003) studied different kinds of manures and reported high nutrient contents in

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poultry manure which increased the yield of tomato. Akande and Adediran (2004) also examined the beneficial effect of manure on tomato and dry matter yield, soil pH, N, P, K, Ca, and Mg and nutrient uptakes. Later, Aluko and Oyedele (2005) studied the effects of organic waste on the physical properties of soil and reported the significance of animal manure on soil density and porosity. Among all organic manure sources, poultry manure was found to be concentrated maximally concerning nutrient content (Lombin et al. 1991), since it mineralizes more rapidly than other animal manure, thereby rapidly releasing nutrients for plant uptake and utilization (Brady and Weils 1999). Senjobi et al. (2010) reported the growth-promoting effect of poultry, plant, and sheep/goat manures in the enhancement of vegetable growth parameters. Similarly, increment in chlorophyll content and grain yield of maize and sorghum was also observed by Amujoyegbe et al. (2007). Although, the application of a supra-optimal quantity of fertilizer proved a suitable strategy for optimizing high productivity (Kumar et al. 2009; Calabi-Floody et al. 2018) quality food nutrients is obtained only by the application of organic manure including dung.

4.8 Effect of the Blending of Organic and Inorganic Fertilizers On the contrary, amendments of organic manure alone may not offer satisfactory nutrient supply (Palm et al. 1997; Gentile et al. 2011; Bedada et al. 2014). To achieve the demand, amendment of a combination of organic and inorganic resources viz. (ISFM, Integrated Soil Fertility Management) outsourced resulting in better yield and nutrient storage (Bedada et al. 2014; Ewusi-Mensah et al. 2015) For instance, a combination of cow dung with NPK, significantly increased the yield of potato tuber (Onwudike 2010). Earlier, combined application of NPK and compost (50 + 50%) influenced the increment in carbohydrate content (Haukioja et al. 1998) and enhancement of tomato and cucumber yield (Marzeh et al. 2012). EI-Sherbeny et al. (2005) observed application of compost showed a remarkable increase in plant pigments and total carbohydrate in Sideritis montana. Such a combination revealed more cobs to borne and increase the crop yield in maize (Ayoola and Makinde 2008; Bedada et al. 2014). The combination of inorganic and organic manure boosted soil organic matter, phosphate availability, exchangeable ions, effective cation exchange capacity, and soil pH (Onwudike 2010) required to increase soil fertility. Earlier, Moyin-Jesu (2007) exhibited that a combination of plant and animal wastes with NPK (15:15:15) increased uptake of N, P, K, Ca, and Mg in coffee seedlings. Earlier, Chand et al. (2006) reported that the mixed use of NPK and organic manure increased N, P, K in soil and the growth of Mentha arvensis and Brassica juncea. Recently, Francioli et al. (2016) observed the integrated use of extremely low dosage of chemical fertilizer along with farmyard manure. The increased soil organic matter, total nitrogen content, and soil microbial biomass carbon (MBC) and crop yield were recorded. Application

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of NPK + cattle manure and NPK + swine manure increased total organic carbon (TOC), total nitrogen, and crop yield, in comparison to NPK fertilization (Li et al. 2017). Further, the combined application of organic (cattle manure compost) and inorganic (NPK) fertilization increased soil organic carbon (SOC), total nitrogen and also improved the bacterial community involved in the breakdown of complex organic matter and in transferring soil carbon, nitrogen, and phosphorus transformations (Li et al. 2019). Some of the properties of nature of organic and inorganic fertilizers are given in Table 4.7. The use of plant nutrients from inorganic fertilizer materials, i.e. N, P2 O5, and K2 O has increased dramatically and the most remarkable increase has been noted in N, P, K, and S. But, the nonrenewable nature of fertilizer raw material is a disadvantage revealed by lack of nitrogen through denitrification. Dung can meet out the plantmineral requirements in the form of compost as nutrient supply occurs via intake from the soil. When the dung was mixed with grassland soil under controlled conditions the size of the soil microbial biomass, respiration rate also increased as supported by Lopes et al. (2010). It is now established that the specific respiration was higher in treated with cattle dung in comparison to that of non-amended soil always, hence acted as good resource for maintaining the status of agro-productivity and improves the beneficial microbial population of soil (Lovell and Jarvis 1996). In few countries, buffalo farms produce extra manure, i.e. dung (Nanda and Nakao 2003) resulting increase in a treasured source of biogas, instead of representing a waste, due to its optimal C: N ratio of about 30 (Yasin and Wasin 2011). Huws et al. (2012) investigated the effects of nourishing sorghum as opposed to maize on rumen microbial diversity. Carillo et al. (2012) studied the microbial diversity and analyzed the community on the manure and also reported the isolation of different eubacteria Table 4.7 Comparison of organic and inorganic fertilizers Basis

Organic

Inorganic

Meaning

It is a natural material, obtained by decaying plant and animal waste, that can apply to the soil to enhance its fertility

It is a human-made or synthetic substance, that can be added to the soil to improve its fertility and increase the productivity

Preparation

Prepared in fields

Products of factories

Humus

It provides humus to the soil

It does not provide humus to the soil

Nutrients

Comparatively less rich in plant nutrients

Rich in plant nutrients

Absorption

Slowly absorbed by plants

Quickly absorbed by plants

Side effect

There is no side effect; in fact it It causes harm to the living organisms, improves the physical condition of soil disturb soil ecology and pollute ground water

Safety

Safe

Harmful

Longivity

Sustainable

Non-sustainable

Cost

Cost effective

Expensive

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microbial communities, after anaerobic fermentation in batch reactors, as affected by the different fermentation conditions.

4.9 Dung in Agrobiological Practices Dung came into focus as a potential antimicrobial agent (Chitnis et al. 2000) against multidrug resistant and Vancomycin resistant bacteria causing human infections. Evidence showed that fresh dung and urine have antifungal and antiseptic properties due to the secretion of some of the antimicrobial metabolites (Nene 2003). Certain phytopathogenic fungi such as Fusarium solani, F. oxysporum, and Sclerotinia sclerotiorum also suppressed by antifungal nature of dung (Basak et al. 2002). Bacterial blight disease of rice was found to be controlled by the spray of dung extract and acts as effective as penicillin, paushamycin, and streptomycin (Mary et al. 1986). The research revealed that Aspergillus niger, Trichoderma harzianum, Bacillus cereus, and Bacillus subtilis inhabiting in dung reduce the growth of Sclerotium rolfsii, F. oxysporum, Pythium aphanidermatum, Helminthosporium maydis, and Rhizoctonia solani. On the other hand, a number of antibiotic resistant strains were also isolated from dung which may act as antibiotic resistant markers in rhizosphere biology (David and Odeyemi 2007). Dung is considered as an integral component of most of the biodynamic preparations and serves as a source of inoculum of beneficial microorganisms (Dhiman et al. 2019). The biodynamic products contain macro and micronutrients, amino acids, and growth-promoting substances like IAA, gibberellins, and beneficial microorganisms. The beneficial effects of biodynamic preparations have been reported on lentil and wheat (Carpenter-Boggs et al. 2000). Biodynamic sprays increased the yields of cereals and vegetables (Raupp and Koenig 1996). In addition, spraying a 3% solution of biodynamic products prepared by dung along with soil application of biogas slurry improved the yields of maize and sunflower (Somasundaram et al. 2007). In agricultural practices, it utilizes as manure because of the presence of humic compounds thus played an important role to increase crop growth (Girija et al. 2013). Low C: N ratio in dung manure is an indication of good source of protein for microbes resides in it and involved in the decomposition of organic matter (Adegunloye et al. 2007). From ancient times, numbers of formulations were prepared either alone or in combination with herbal, animal, or mineral origin drugs (Sathasivam et al. 2010). Farm animals such as cows, bullocks, and milk buffaloes provide dung and urine to enrich the soil, while crop residues and fodder form the bulk of the feed for these animals (Kesavan and Swaminathan 2008). Studies revealed that dung remained the most important source of bio-fertilizer and at the same time urine, horn, and dead bodies can be the sources for effective bio-fertilizer. In mixed farming systems, most livestock products are derivatives of animals that fed on local resources such as crop residues, pasture, fodder trees, and shrubs. In India, farming and agricultural cultivation is used to be done with animal dung and serving as manure as per the traditional age-old system. There are a variety

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of animal dung and urine products, which can be used as fertilizers and pest repellent, respectively (Katzen 1978). Recently, in India, dung soaps, paper, and dyes have been introduced due to beneficial properties toward skin infections and other dermal diseases (https://www.amarujala.com/business/business-diary/nitingadkari-launches-soap-made-from-cow-dung-and-bamboo-bottles). These dungbased commercial products and their microbiota are widespread and being augmented for the sustainable plant-soil ecosystem. Acknowledgements The authors gratefully acknowledges the Department of Botany and Microbiology, Gurukul Kangri University, Haridwar for providing all the infrastructural facilities to carry out this research.

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Chapter 5

Fluorescent Pseudomonads in Iron Chelation and Plant Growth Promotion in Abiotic Stresses C. Dileep, C. G. Sreekala, T. S. Reshma, and Surabhi Sankar

Abstract Iron is an essential nutrient for plant growth and plays a pivotal role in the energy metabolism of plants. But abiotic stress such as soil salinity is a leading cause of iron limitation by excessive acquisition by plants. Soil salinity arises as a result of climatic changes and it will be one of the major threats to crop production. It affects the soil characteristics and thus the nutrient uptake for plant growth in saline soils. Plants and microbes overcome this iron limitation by producing iron-chelating agents known as Siderophores. Fluorescent pseudomonads are being considered as most promising organisms which are free-living and endophytic nature, hence be exploited as potential iron chelators of sustainable solution for plant health management. Effect of Iron on siderophore production, pH levels, antagonism, and root colonization are crucial factors which are found to be effective for raising crop in sustainable manner. In the presence of Iron, their fluorescence is masked due to the formation of the siderophore complex. Thus, iron deficiency induces siderophore production and root colonization of such efficient native strains, ensures nutrient uptake, and promotes plant growth. Keywords Siderophore · Antagonism · Root colonization · Pseudobactin · Pyoverdin

5.1 Introduction Agricultural productivity is curtailed by various types of biotic and abiotic stresses. Salinity stress is one of the major abiotic stresses among them. Climatic changes accelerate the process of soil sanitization. The biological properties of the soil are potentially affected by climatic changes (Patil 2018). Fluorescent pseudomonads are the most promising group of plant growth-promoting rhizobacteria (PGPR) involved C. Dileep (B) · C. G. Sreekala · T. S. Reshma · S. Sankar Department of Post Graduate Studies and Research in Botany, Sanatana Dharma College (University of Kerala), Sanatanapuram P.O., Alappuzha 688003, Kerala, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_5

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in biocontrol of plant diseases (Gardner et al. 1984). Various species mainly Pseudomonas fluorescens, Pseudomonas aeruginosa, Pseudomonas aureofaciens, Pseudomonas putida, and Pseudomonas pyrrocinia demonstrated florescent with varying degrees of the antagonism (de Weger et al. 1986). Some of the fluorescent pseudomonads have currently received world-wide attention due to the production of a wide range of antifungal compounds (Minaxi and Saxena 2010); siderophores; volatile compounds such as HCN (Defago and Haas 1990), antibiotics such as phenazine-1-carboxylic acid; pyoluteorin (Hu et al. 2005); viscosinamide and tesin (Chin et al. 2003); 2,4-diacetylphloroglucinol (Shanahan et al. 1992); and lytic enzymes. The suppression of phytopathogens depends on the ability of the bacteria to colonize the roots and production of an antibiotic phenazine-1-carboxylic acid (PCA), siderophores, and some antifungal factor (AFF). Iron-regulated, non-siderophore antibiotics may be produced by fluorescent pseudomonads more frequently than previously recognized, and could be partly responsible for beneficial effects that were attributed in the past to fluorescent siderophores (Thomashow and Weller 1990). This will lead to the nutrient imbalance in the soil. The high pH and high T.S.S (Total Soluble Salts) creates a complex microenvironment in the rhizosphere. The nutrient uptake by plants will be challenged in this environment and adversely affects crop productivity (Chaudhari et al. 2013). Iron is one of the essential micronutrients and its availability to plants is limited by its non-solubility in soil. Salinity increases the non-solubility of the iron. Iron limitation in saline soil is a multistress condition (Ferreira et al. 2019). PGPR proved effective in stress alleviation and can be modified rhizosphere by these organisms (Backer et al. 2018). The fluorescent Pseudomonas, a reliable game-changer of iron chelation by siderophores converts insoluble iron into available form for plant-uptake (Bakker and Schippers 1987). This chapter focuses on the mechanism of plant growth-promoting fluorescent Pseudomonads to avoid iron limitation and assist in facilitation for the growth and development of plants.

5.2 Interaction Between Deleterious Rhizo Bacteria (DRB) and PGPR Seed bacterization with fluorescent rhizosphere pseudomonads suppressed deleterious (growth-inhibiting) rhizosphere bacteria (Geels et al. 1983, 1985; Kloepper and Schroth 1981; Schippers et al. 1985; Schroth and Hancock 1982; Suslow 1982; Suslow and Schroth 1982). This draws support from the fact that growth promotion is accompanied by a decrease in the number of rhizosphere microorganisms that when reintroduced in the rhizosphere are found to adversely affect the root growth (Suslow and Schroth 1982). The suppression of DRB and the yield decrease is the result of at least two properties, (i) fluorescent pseudomonad isolates interfere with the iron metabolism in the soil by converting Fe3+ ions to a form, by complexing

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with its siderophore, which cannot be used by harmful DRB, resulting in a decrease in their number and activities, and (ii) to the harmful microorganisms effectively, the fluorescent pseudomonads must be capable of colonizing and thus protecting the whole root system of the plant. The interactions between the DRB and PGPR as mediated by siderophores are depicted in Fig. 5.1. When the DRB colonize the roots they produce HCN from a rhizosphere metabolite using iron from the surrounding soil environment with the siderophores they produce. The HCN affects the energy metabolism and the consequent loss of uptake of essential elements like N, P, and K. Cyanide production is thus dependent on the availability of iron (Fe3+ ). The PGPR first hit here by scavenging all the Fe3+ availability by their more efficient siderophores and also by their capability to use the siderophores of the DRB also. Thus, the interaction is competition for Fe3+ and the iron starved DRB lose their hold on the root yielding place to the PGPR. The absence of DRB and hence the nonproduction of HCN explain the release from growth suppression (Dileep and Dileepkumar 2000). It is interesting to note that the designation “growth promotion” or “crop yield increase” is applicable only in the short rotation of crops. All strains

Fig. 5.1 Interaction between Deleterious Rhizo Bacteria (DRB) and PGPR

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have common property of antagonism against Gram-positive and Gram-negative pathogenic bacteria and this gives the “double-action” of PGPR—they control the pathogens and thus control disease, besides adding to growth and yield. This antagonistic activity is exerted usually only when the iron is deficient, as only under conditions of iron limitation the PGPR produce the siderophores that chelate the iron. Thus, the term PGPR is a misnomer because their action is by antagonism of deleterious bacteria or “minor pathogens” rather than as plant growth promotor as such. What happens is the removal of growth inhibition, rather than growth promotion. Hence, something is to work against as infrequently or over-cropped potato soils where about 50% of Pseudomonas isolates observed deleterious, and not in sterile soils or when the DRB are absent. Thus the modus operandi for plant growth promotion is competition for iron supported by the following in vitro experiments (a) addition of dissolved iron (Fe3+ ) to the environment abolishes in vitro antagonism and also prohibits the plant growth promotion by PGPR strains and (b)siderophorenegative mutants, obtained by exposure of wild type of PGPR strains to UV light or mutagenic chemicals or obtained by transposon mutagenesis, also lost their PGPR activities, although they colonized roots as well as similar to the wild type PGPR (Bakker et al. 1987).

5.3 Iron Deficiency and Siderophore Production Iron is an essential element for living organisms under its two stable valences that act as cofactors in various oxidative-reductive enzymatic reactions. Although iron is abundant, comprising 4–5% of the average soil, iron deficiency of crop plants is common in calcareous soils that represent over one-third of the world’s land surface area. In well-aerated soils with a high pH, the concentration of Fe2+ and Fe3+ becomes negligible. The concentration of chelated iron required for optimal growth is of the order of 10−6 –10−5 M. Cultivars that grow in alkaline soils without developing symptoms of lime-induced chlorosis are called “iron efficient” while those that become “chlorotic” are iron-defficient. Fe is reflected by the number of mechanisms developed by plants and microorganisms for its acquisition. Plants undergo in iron deficiency overcome by several mechanisms: (i) secretion of protons by roots (Marschner et al. 1974) (ii) secretion of reducing compounds by roots and (iii) secretion of phytosiderophores (Suguira and Nomato 1984). Although, phytosiderophores are widely distributed in higher plants (Rippenger and Schreiber 1982), they have only been isolated from root washings of graminaceous plants. These are amino hydroxyl carboxylates with high affinity for Fe3+ (Kf 10s) although not as high as those possessed by bacterial and fungal siderophores. Besides, plants’ supporting fluorescent pseudomonad flora is a mechanism to make iron available to itself (Dileep and Dileepkumar 2000). Microorganisms have evolved efficient uptake systems to obtain sufficient amounts of iron. Most aerobic and facultative aerobic bacteria possess a highaffinity iron-transport system in which siderophores are excreted and the consequent

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iron complex is taken up via the cognate-specific receptor and a transport pathway (Neilands 1981; Neilands et al. 1987). Microorganisms have developed following methods of iron acquisition, membrane-bound chelator (Royt 1988), and reduction of iron chelates (Emery 1987; Lesuisse and Labbe 1989; Zimmermann et al. 1989).

5.4 Siderophores The production of siderophores by microorganisms in slightly acidic, neutral, or alkaline soils is a general phenomenon (Kloepper et al. 1980) . No system analogous to the siderophores has been found for any other metal ion and Fe3+ seems to be unique in requiring such specific ligands. Siderophores are low molecular weight iron-chelating agents produced by virtually all bacteria and fungi under iron-limiting conditions. The fluorescent pseudomonads producing siderophores (water-soluble, yellow-green fluorescent pigments) viz. P. aeruginosa, P. putida, and P. fluorescens all belong to the same inter-generic homology group (Palleroni et al. 1973; Palleroni and Doudoroff 1974). Turfreijer (1942) proposed the term “pyoverdine” for the pigment of P. fluorescens by its analogy with that of phenazine pigment, pyocyanine produced by P. aeruginosa. The term pyoverdine has been extended to include all pigments produced by fluorescent pseudomonads. However, due to differences in structure, these are now named differently. Mayer and Abdallah (1978) like to designate the pigments of this class by a suffix including the species responsible for their production e.g., pyoverdine Pf for the pyoverdine of P. fluorescens. The main differences observed between those produced by different strains are the number, composition, and sequence of their L- and Damino acids which are thought to give the molecule their receptor specification (Hohnadel and Mayer 1988). During the past years, the chemical structure of a large number of microbial siderophores has been elucidated by NMR spectroscopy, Mass spectroscopy, Chemical degradation, and X-ray diffraction. Two different names have been used for siderophores of Pseudomonas sp. pyoverdine, and pseudobactin. The complete structure for pseudobactin, the siderophore of Pseudomonas BlO, has been determined. It consists of a linear hex peptide: L-Lys-D-Threo-BOH-Asp-L-Ala-D-allo-Thr-L-AlaD-N-OH-Orn, in which the ornithine residue is cyclized into an N-hydroxypiperidone ring and the lysine residue, is linked to a fluorescent quinoline derivative. The iron chelation to the hydroxamate, the a-hydroxy acid, and the -o-dihydroxy group1, establishes pseudobactin as one of the unique groups of siderophores. The occurrence of both L- and D-amino acids is also unusual and their alternate sequence in pseudobactin explains why the compound is not affected by proteolytic enzymes. The pyoverdine for P. fluorescens has been partially characterized. It contains seven amino acid residues with two hydroxamate groups and an o-dihydroxy aromatic group. The complete structure of pyoverdine Pa from P. aeruginosa has been determined (Dileep et al. 1998).

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All the siderophores in this family are related by having a cyclic or linear peptide containing D- and L- amino acids, mixed ligand groups with at least one hydroxamate group or and a-hydroxy acid. Structurally at least eight amino acid residues are required for cyclic compounds. Even different strains of the same organism produce different pseudobactins which are discriminated in the uptake process of the various strains. The affinity of siderophores for Fe3+ is expressed as a binding or stability constant log 10 K Fe (pH 7.0). It is pH-dependent, varies widely among the various siderophores, and is thus an important ecological factor in the microbial competition for iron. The solubility of organic iron might be relative to the soil type (Benjamini and Hochberg 1995). Iron is more soluble and biologically available at low pH (Wandersman and Delepelware 2004). Increasing pH siderophore production ceased, this may be since alkaline pH help in excess solubilization of iron, which increases the iron content of the soil. Acidity affects metal speciation and bio-availability to microbes through various mechanisms (Lofts et al. 2004; Gobran and Huang 2011). P. aeruginosa species from acidic soil shows siderophore production in iron-deficient succinate medium in varying degree of absorbance and peaks. A potent siderophore, such as the ferric-siderophore complex plays an important role in iron uptake by plants in the presence of other metals, such as nickel and cadmium (Beneduzi et al. 2012).

5.5 Plant Responses to Salinity The ability of the plant to the saline environment depends on its genetic makeup and physiological responses. Cereals and vegetables are very sensitive to salinity (Paul and Lade 2014). Plant response to salinity starts by the osmotic adjustments and later by the specific ion effects. High salinity causes structural and functional impairments in plants and affects crop productivity (Meng et al. 2017). Plants exposed to salinity show stunted growth, delay or absence of germination, low seedling growth, decrease in root length, and root meristems (Ameixa et al. 2016; Konuskan et al. 2017; Taibi et al. 2016; Acosta-Motos et al. 2017). Salt stress creates nutrient imbalances (Grattan and Grieve 1998). Physiological responses to salinity results in the reduction of crop production by altering the protein synthesis, photosynthesis (Pessarakli 2014).

5.6 Unavailability of Iron in Saline Soils Limited iron availability in soil is one of the leading causes of a reduction in crop productivity. Iron is playing a key role in photosynthesis, electron transport, enzymatic processes involving oxygen (Ferreira et al. 2019). Iron catalysis the chlorophyll synthesis (Hu et al. 2017) and is the second most abundant metal in the earth’s crust; rather it is not accessible to plants. This is due to the insolubility of Iron. Fe2+ and

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Fe3+ are the two interconvertible forms of iron; pH, salinity, and alkalinity influence the conversion of Fe2+ and Fe 3+ . Iron combines with phosphates, carbonates, calcium magnesium, and hydrogen ions and its limitation increases due to its non-solubility corresponding to salinity. The downregulation of iron transportation in response to salinity may lead to iron limitation (Cotsaftis et al. 2011). Another context of a reduction in iron availability is the inhibition of proton pumps required for the uptake processes (Rabhi et al. 2007).

5.7 Avoidance of Iron Limitation in Saline Soils Plants under iron deficiency exhibit various mechanisms to avoid the Iron limitation. This is also including root exudates and phytosiderophores production. Bacterial siderophores are more efficient when compared to phytosiderophores and efficient siderophores have been observed in different genera of plant growth-promoting rhizobacteria which can avoid deleterious phytopathogens (Dileep 2012). The root exudate secretions and other metabolites include amino acids, organic acids, and phenolic compounds which lower pH of the soil and avoid to interfere iron availability. These root exudates attract the PGPRs to the rhizosphere regions by root colonization and chemotaxis, thus facilitate to chelate iron (Singh et al. 2010; Aeron et al. 2020). The iron-siderophore complexes, having membrane receptors, can easily access the Iron. Iron limitation in saline soils can be alleviated through the inoculation of halo-tolerant PGPR as given in Fig.5.1.

5.8 Fluorescent Pseudomonads—A Sustainable Solution for Iron Limitation in Saline Soils The effective strategy for avoiding Iron limitation by the application of P. fluorescens, P. stuzeri on Tomato (Tank and Saraf 2010), on common bean by P. fluorescens (Younesi and Moradi 2014); Growth promotion reports on Groundnut by P. fluorescens (Saravanakumar and Samiyappan 2007), and in Peanut (Sharma et al.2016) and various other crop plants (Maheshwari 2011; Maheshwari et al. 2013). In a case study, saline tolerant fluorescent pseudomonads are collected from the saline Pokkali rice field, with an average 5.9 pH and 5.0 T.S.S (Total soluble salt). Pokkali is a salt-tolerant, GI tagged rice variety; cultivated in saline soils. The primary screening of the organism, by its ability to fluorescence under UV light. The King’s B medium (Peptone 20 g; MgSO4 .7H2 O 1.5 g; K2 HPO4 1.5 g; Agar 15 g; Distilled water 1L) is modified by varying concentrations of NaCl to screen the salt tolerance of the organism. Selected strains are inoculated in iron-deficient, synthetic, succinate medium (Mayer and Abdallah 1978), incubated for 48 h at 30 °C. The culture supernatants were centrifuged at 10000 rpm for 20 min. The supernatants were filtered

112 Table 5.1 Siderophore production in Pseudomonas isolates

C. Dileep et al. Bacterial strains

Incubation period (h)

Peak

Absorbance

P6 1

48

404

0.788

PK7

48

403

2.137

Fig. 5.2 Absorbance spectra of Pseudomonas isolates

and measure OD at 300–600 nm in UV Visible spectrophotometer (SHIMADZU UV 2600), to measure the siderophore production. Obtaining a peak at or near 404 nm indicates the presence of siderophore (Table 5.1; Fig. 5.2). The graph shows a clear peak at 404 nm by the strain P6 1 and the strain PK 7 shows the same at 403 nm. These two strains belong to fluorescent pseudomonas and can be considered as a reliable source of siderophore. Also, they produce phytohormones, ACC-deaminase, enzymes, etc. The increase of shoot and root length and promotion in the early vegetative growth parameters were observed (Da Silva et al. 2018). The number of roots and its length is significant in iron uptake. These two are directly proportional to each other (Fig. 5.3). The crop protection under salinity can be well played by fluorescent pseudomonads. Considering all these facts, the exploitation of these microbes and its application in saline soils ensure the sustainable strategy for Iron chelation and plant health management.

5.9 Root Colonization and Plant Growth Promotion Root colonization study of acidic tolerant Pseudomonas species Rhizobacteria can indirectly lead to reduced pathogen attack through induction of systemic resistance (Kloepper and Beuchamp 1992). Colonization of roots by inoculated bacteria is an important step in the interaction between beneficial bacteria and the host plant

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Fig. 5.3 Effect of salinity on PGPR activity

(Benziri et al. 2001). The use of naturally occurring rhizobacteria, which protect and promote plant growth by colonizing and multiplying in the rhizosphere/root cortex, could be an alternative method for plant protection. Rhizobacteria and especially the fluorescent pseudomonads have emerged in the last two decades as organisms of great importance that modulate the growth of plants by providing freedom from growth inhibition of deleterious rhizosphere microorganisms and, thus, restoring normal growth and yield. Under being antagonistic to some major pathogens they also provide “biological control” which is more eco-friendly and needs of the time in face of a threat from pollution by the use of chemical disease-controlling agents (Dileep Kumar and Dube 1992). Nature practices biological control as evidenced by the existence of disease suppressive soils for various diseases. We have only to learn nature’s ways and try to simulate or support it. Their study has injected anew interest in plant microbial interactions in recent years. The plant growth-promoting substance produced by P. fluorescens might have exerted a synergistic action and enhanced the growth promotion of seasonal crop plants. Pseudomonas spp. were reported producing amino acids, salicylic acid, and IAA (Sivamani and Gnanamanickam 1988; O’ Sullivan and O’ Gara 1992). Growth promotion studies of acidic tolerant strains show a high rate of plant growth promotion which might have improved the plant growth and seedling vigor. PGPR is an ecofriendly tool for keeping soil fertility by nutrient enrichment. The production of secondary metabolites change the root architecture and enhance the nutrient uptake and provide the opportunity to enhance the beneficial effects of PGPR (Table 5.2).

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Table 5.2 Data represent values of 5 replicates of 15 plants. Data in parenthesis represent percentage over control Treatments

Germination (%)

Shoot (length in cm)

Root (length in cm)

Fresh weight (g)

Dry weight (g)

RP12 + Rice

98.1 (11)

18.76 (49.59)

10.43 (34.94)

1.237 (40.9)

0.199 (91.8)

MIP + Rice

95.8 (8.87)

18.53 (48.96)

8.32 (18.44)

1.5048 (51.42)

0.182 (15.6)

FPO4 + Rice

93.8 (6.9)

14.744 (35.86)

6.17 (9.96)

0.765 (4.44)

0.173 (11.21)

Control

87.3

9.456

6.785

0,731

0.1536

5.10 Effect of Iron and PH Levels FeCl3 amended media were fluorescent. In the case of pH, the results varied in different media. The strains were capable of producing siderophore even in an extremely acidic pH of 4.2 being isolated from the acidic fields. The use of resident organisms is advocated over the alien ones as the formers are well adapted to the prevalent edaphic and agroclimatic conditions (Fonseca-García et al. 2016). Based on these findings it is clear that root exudates, pH, and the presence of FeCl3 are major factors in the rhizosphere that influence growth, metabolic production, and root colonization of the microflora.

5.11 Effect of Iron on Antagonism The effect of iron on antibiosis by the four maximally inhibitory organisms was examined by the “dual culture test” suggested by Utkhede and Rahe (1983) on the Kings B Medium. No effect on inhibition by iron inclusion in the medium will mean noninvolvement of siderophore and a change in inhibition would suggest the involvement of siderophore (Andrews et al. 2003). It was noted that in all cases the addition of iron curtailed fluorescence, siderophore production caused a reduction in their inhibition of the test fungal pathogens. The inhibition ranged varied for the test fluorescent pseudomonads as, P6 1, 22.3–68.4%; RP12, 32.3–70.0%; PK12, 11.8–77.8% and MIP shown 18.2–64.3%. The loss in inhibition is quite appreciable which points out to involvement of siderophores in the growth inhibition of the fungal pathogens. The role of other chemicals is not ruled out.

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5.12 Influence of Amino Acids, Organic Acids, and Sugars on Growth, Fluorescence, and Siderophore Production The organic substrates in the rhizosphere lead to greater growth and activity of the microorganisms around the roots. The influence of amino acids, organic acids, and six sugars, commonly encountered in root exudates showed siderophore production, plant growth promotion, and disease suppression. Among the eight amino acids tested (L-alanine, D-L-arginine, L-glutamine. L-lysine, D-methionine, D-L-proline, D-L-serine, L-tyrosine) for growth of the organisms, amino acids (methionine and serine) did not support the growth of any of the organisms and thus were not an energy source for these bacteria (Dileep et al. 1998). Among the rest six amino acids, three (L-alanine, D-L-proline, and L-tyrosine) supported both growth and fluorescence. Six organic acids screened were L-aspartic acid, citric acid, D or L-glutamic acid, L (+) lactic acid, D-maleic acid, and succinic acid that supported growth curtailing fluorescence and not supported siderophore production. Arabinoses among several sugars not supported growth and it supported only growth (not fluorescence) of the rest two organisms. It is interesting to note that in the presence of sugars (except glucose) the siderophore production was arrested (Dileep et al. 1998). Thus, sugars do not support siderophore production. But keeping in view the ubiquity of glucose, it does not affect much in nature (Table 5.3).

5.13 Siderophores as Iron Storage Compounds Although siderophores were identified and confirmed as iron transporting agents, there is evidence that they may have further intracellular functions. Several spectroscopic studies confirmed the possible involvement siderophores on iron storage (Kraemer et al. 2006). Recent research on the occurrence of siderophores in P. aeruginosa has indicated well-known hydroxamate type Siderophores. Uptake of iron-mediated by siderophores is energy-dependent and requires the specific interaction with siderophores is transport systems in the cytoplasmic membranes. Iron from siderophores is transported to the cellular metabolism by a reductive removal, which is not operating in the corresponding aluminum, chromium, or gallium complexes (Römheld and Marschner 1986). Transport studies using various hydroxamate type siderophores revealed that the absolute configuration of the metal center, the number, and kind of irons surrounding N-acetyl residues and the overall structure of the various hydroxamate families. Besides the function in iron chelation and transport, the third function in iron storage has recently been confirmed by the hydroxamate siderophores.

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Table 5.3 Influence of various root exudates on growth, fluorescence, and siderophore production of two fluorescent Pseudomonas Growth and fluorescence

Siderophore production (ODa )

P61

RP12

P61

RP12

L-alanine

+

+

0.201

0.370

L-glutamine

NF

+

0.313

0.132

L-lysine

NF

NF

0.071

0.063

L-tyrosine

+

+

0.275

0.314

Substrate Amino acids

D-methionine

NG

NG

NT

NT

D-(L)-arginine

NF

+

0.085

0.164

D-(L)-proline

+

+

0.497

1.279

D- (L)-serine

NG

NG

NT

NT

L-aspartic acid

+

+

0.271

0.285

D-maleic acid

NF

NG

0.000

0.000

Succinic acid

+

+

0.151

0.080

Citric acid

NF

NG

0.000

0.000

D/L-glutamic acid

NG

NF

0.000

0.202

L (+) lactic acid

NG

NG

NT

NT

D (−) fructose

NF

+

0.000

0.000

D (+) mannose

+

NF

0.000

0.000

D (−) galactose

NF

NF

0.000

0.000

D (−) ribose

NF

NF

0.000

0.000

D (+) glucose

+

NF

0.362

0.023

L (+) arabinose

NG

NG

0.000

0.000

Organic acids

Sugars

+ = growth with fluorescence; NG = no growth; NF = Growth with no fluorescence; NT = not tested a Absorbance at 404 nm after 48 h

5.14 Conclusion and Future Aspects Soil rhizosphere competence for Fe is supposed to be controlled by the Fe affinity of the siderophores, which is the hexadentate ligand produced by the fluorescent pseudomonads in higher concentration than the pathogen. In this study we found that a notable proportion of rhizosphere and rhizoplane soil fluorescent pseudomonads are able to make use of the Fe in pure or complex form of the hydroxamate siderophores as an Fe source. The Fe-siderophore could be utilized by most of the strains isolated and their ability to scavenge the siderophore produced by other microorganisms conferring an ecological advantage.

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Competition for Fe can be considered as occurring in two stages (a) competition for the metal by the siderophores and (b) competition between the microorganism particularly fluorescent pseudomonas for the Fe-siderophore complex, The former is controlled by proton dissociation and formation constant of each siderophores as well as by their concentration and kinetics of exchange, while the latter is governed by existence of an uptake mechanism for, and its affinity to, the Fe complex (Edouard et al. 1992). Soil salinity and acidity also alter the soil characteristics which negatively affects the Fe uptake of pseudomonads, which influence the nutrient uptake of plant community. Saline and acidic tolerant pseudomonads have to compensate in this with improved osmo-tolerance and could play a pivotal role in the benefit to the plants grown in saline soils, in better growth, colonization, and yield. A potential application of microbial inoculants to improve crop growth and yield in saline environments is a potential strategy for saline soil agriculture. Plant root exudates mainly amino acids, organic acids, and sugars have a positive role in colonization of fluorescent pseudomonas in the microenvironment of the plant root system. A consortium of different PGPRs with known functions that could act symbiotically as they offer multiple modes of action, with variability. The data presented in this article supports that some saline acidic tolerant pseudomonads which are intrinsically less available to rhizosphere utilizes the Fe in faster rates with their siderophores which is an important finding as one of the parameters in reducing the availability of Fe to other microorganisms in the rhizosphere. Interaction between these soil fluorescent pseudomonads colonizing on the rhizosphere and rhizoplane of plant root system will progress to harness, thus, improving the general health growth, yield of the plant, and overcoming the stress.

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Part II

Endophytes and Mineral Nutrition

Chapter 6

Microbial Endophytes: New Direction to Natural Sources Azim Ghasemnezhad, Arezou Frouzy, Mansour Ghorbanpour, and Omid Sohrabi

Abstract The concept of endophytes and their beneficial relationship with the plant is widely accepted as an important step in the co-evolution and diversity of plants. The symbiotic relationship between plants and fungi and rhizobia with legumes have a long evolutionary history. During exploration, fossils have shown close associations between endophytic fungi and plants roughly, 400 million years ago. The common symbiotic relationship between fungi and plants facilitated the evolution of large group of primary and secondary metabolites of considerable chemical diversity, have a unique structure and high biological activity. During the last two decades, a growing interest in the study of endophytes, origin, biodiversity, interactions between endophytes and host plants, their role in ecology as well as biological activities of metabolites have been established. Several novel and beneficial activities for these microorganisms are evident by available literature, reveals their role as multifarious biologicals. The diversity and dynamics of endophyte populations, use of microbial inoculants to improve plant growth and health, and their role as a new bio-resource for metabolites are considerable interests of the twenty-first century. The exploration of active secondary metabolite is one of the most important reasons for the endophytes of industrial significance. Keywords Ecology · Bacteria · Endophyte · Fungi · Metabolites · Symbiosis

A. Ghasemnezhad · A. Frouzy Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran M. Ghorbanpour (B) Department of Medicinal Plants, Faculty of Agriculture and Natural Resources, Arak University, Arak 38156-8-8349, Iran e-mail: [email protected] O. Sohrabi Department of Horticultural Sciences, Guilan University, Rasht, Iran © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_6

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6.1 Introduction To understand why endophytes have received great attention in the field of antimicrobial research, there is a need to examine their intended role in nature. Microbial groups residing in plant tissue have been identified as symbiotic or pathogenic (Larran et al. 2016; Martinez-Klimova et al. 2017). According to Wilson (1995), endophyte (Gr. Endon, within; Phyton, plant) is an organism that lives within the plant. Usually, the organisms found inside the plant are fungi and bacteria. Endophytic host plants show no signs of disease symptoms at least during the endophytic phase of their life cycle (Wilson 1995). Endophytic fungi are found in all plant families worldwide and almost in all climatic conditions (Larran et al. 2016; Martinez-Klimova et al. 2017; Santoyo et al. 2016). Microbes enter plant tissues through wounds or roots or the creation of wounds by secreting enzymes such as pectolytic and cellulolytic enzymes. It is unclear, why plants and endophytes co-exist or why plants do not defend themselves against internal colonization (Martinez-Klimova et al. 2017; Wilson 1995) yet to be understood. So far, the relationship between plant co-existence and endophyte seems to be beneficial to both parties and has dual advantages. It is beneficial for endophyte due to plant nutrients and habitat while for the plant because of the protection against pathogens, increased nutrient uptake, plant growth promotion (Martinez-Klimova et al. 2017; Santoyo et al. 2016) and stress resistance (Larran et al. 2016) Bacterial endophytes facilitate the acquisition of essential mineral nutrients through the environment such as nitrogen, phosphorus, and iron (Zhang et al. 2006; Gangwar et al. 2014) and also produce vitamins or modulate phytohormone levels in the plant because of their nature of producing auxin, cytokinin, gibberellins, etc. (Santoyo et al. 2016). Endophytes increase the root volume of the plant (Zhang et al. 2006), and increased plant growth thus, may eliminate the cellular apoptosis caused by the pathogen infection (Alvin et al. 2014). However, according to Hyde and Suetong (2008), more research is yet to be done to confirm the beneficial properties of endophytes toward plants. Endophytic plants are believed to be healthier than non-endophytic plants (Zhang et al. 2006), because endophytes produce metabolites that promote plant growth and protect the plant, act against insects, pests, and plant diseases (Golinska et al. 2015; Abdalla and Matasyoh 2014). Since, the natural products of endophytes act as antimicrobial, antifungal, anticancer, and antioxidant agents as reported by Zhang et al. (2006), hence, secondary metabolites produced by endophytes might be useful in the pharmaceutical industries (Golinska et al. 2015) (Table 6.1; Fig. 6.1). Endophytes are capable of biosynthesis of some chemical compounds like their host plant, possibly as an adaptor to the host micro-environment (Zhang et al. 2006). The most common example is taxol, but several other anticancer compounds such as comptotcin and podophylotoxine have also been reported (Alvin et al. 2014). Endophytes secrete antibiotics and hydrolytic enzymes to prevent the colonization of plant pathogenic microbes or to prevent insects and nematodes penetration and produce metabolites capable of activating the plant defense mechanism or enhancing plant growth (Fig. 6.2).

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Table 6.1 Benefit of endophyte and plants in coexistence Endophyte

Host-plant

Feeding by host plant

• • • • • • • • • • •

Protection against pathogens Increased nutrient absorption Promoting plant growth Stress resistance Nutrient uptake such as nitrogen, phosphorus, and iron Production of vitamins Modulation of auxin, cytokinin, and gibberellin Increase the amount of root of the plant Compensate for cellular apoptosis caused by pathogen infection Preventing colonization of plant pathogens Preventing the penetration of insects and nematodes

Fig. 6.1 Effect of endophyte on biomass and artemisinin production of in Artemisia (Hussain et al. 2017) Fig. 6.2 Influence of endophyte on root growth in rice plant (Korzekwa 2015)

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Thus endophytes try to eliminate apoptosis of infected tissue (Alvin et al. 2014). Induction of plant defense mechanisms by endophyte against pathogens is an attractive phenomenon and acts as control tool used in modern and sustainable farming methods (Martinez-Klimova et al. 2017).

6.2 What Is Endophyte? The most important use of the term ‘endophyte’ is for microorganisms whose intrusions are intangible (Kobayashi and Palumbo 2000). Although, their origin dates to the nineteenth century, its contemporary meaning differs from its original meaning (Carroll 1986). Today’s applications of this term have not been consistent and none have been accepted by all researchers. The definition has changed many times and numerous terms and definitions of endophytic fungi have been proposed by researchers. Carroll (1986), identified endophytes as cooperative fungi that occupy the aerial parts of living plant tissues, but do not cause any symptoms. This definition does not include plant pathogenic fungi and mycorrhizal fungi. Endophytes are closely related to plant pathogens but are of limited pathogenicity and may have evolved from plant pathogenic fungi. Petrini (1991) proposed a broader definition of endophytes than Carroll’s definition, which includes all living organisms living in plant organs and can partially occupy host plants without pathogenic effect. According to this definition, endogenous plant pathogens that live within the host tissue without symptoms, and have an epiphytic phase in their life cycle, are also endophytes. Wilson (1995) defined endophytes as fungi or bacteria that invade living plant tissues throughout or part of their life cycle and induce completely non-obvious, symptomatic, infection within the plant tissue. On the other hand, Sikora et al. (2007) noted that, endophytic fungi reside within the plant tissue and are useful for their host or have no effect on their host. A special term, ‘endophyte’ is used when we refer to microorganisms present in plants. They could be considered as bacteria or fungi or actinobacteria, which spend their whole or part of their life cycle in the inter or intracellular tissues of different plant parts (stems, petioles, roots, leaves) without causing any apparent diseases to their host plants (Singh 2019). According to the researchers, endophytic fungi have three classes. The first category is the pathogenic fungi that are in their non-pathogenic form in the other host plant, the second group belongs to fungi that are generally pathogenic, and the third group has mutated and become non-pathogenic fungi for example, Colletotrichum magna (Backman and Sikora 2008). In general, the definition of the term endophyte is varied in articles and books that have ever been published. But most mycologists use the term for fungi that can occupy living and internal host tissues and do not cause visible disease symptoms (Petrini 1991; Wilson 1995). Endophytes are microorganisms (mostly fungi and bacteria) that live in the interstitial and intracellular areas of healthy plant tissues at a specific time and can colonize without harming the host (Bacon et al. 2000; Strobel and Daisy 2003; Khan 2010). The presence of endophytes in plan ts can alter the food cycle and symbiotic composition,

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ecosystem processes and are important for the structure, function, and health of the plant community (Molina-Montenegro et al. 2015) (Table 6.2).

6.3 Classification of Endophytic Fungi Fungal endophytes are a diverse group of microorganisms that are broadly divided into two groups, clavicipitaceous (C) and non-clavicipitaceous (NC) based on their life cycle, evolutionary dependence, host plant range, and ecological class function (De Silva et al. 2019). On the other hand, Clavicipitaceous endophytes (family of Clavicipitaceae) including Atkinsonella, Balansia, Balansiopsis, Echinodothis, Epichloe, Myriogenospora, Neotyphodium, and Parepichloe are usually associated with the herbaceous plants of the Poaceae family (De Silva et al. 2019). Nonclavicipitaceous endophytes such as Fusarium sp., Colletotrichum sp., Phomopsis sp. and Xylaria sp. are associated with several plants and does not spend their complete life cycle inside the host plant (De Silva et al. 2019; Rodriguez et al. 2009; Jayawardena et al. 2016). A significant attention on endophytes includes various disciplines because of their ability to switch between endophytic, pathogenic, and saprophytic lifestyles (De Silva et al. 2019; Rodriguez et al. 2009) (Table 6.3). Clavicipitaceous endophytes, live as intracellular symbionts are mainly transmitted from mother plants to off-spring and systematically grow in the leaves and stems, by vertical transfer from the mother plant to their off-spring. The off-spring are seed-borne and have systemic growth within the plant’s tissues (De Silva et al. 2019; Arnold et al. 2003; Santangelo et al. 2015). In contrast, endophytes associated with the foliage of woody plants are transmitted horizontally by sexual or asexual spores (De Silva et al. 2019; Arnold et al. 2003). The above examples confirm about the importance of endophytic fungi that are biological control agents. The next important question arises how endophytes reduce disease and pests.

6.4 Plant Defense Responses in Relation to Endophyte-Pathogen and Host Plant Sustainable agriculture can be achieved by reducing or eliminating chemical fertilizers and agrochemicals, which are resulting in harmful environmental impact. Recently, application of antagonist endophytes as biological control agents (BCA) has gained momentum and received special attention for plant diseases management with comparatively low negative impacts on the environment (De Silva et al. 2019). Symptom-free colonization of endophytes can be explained by the hypothesis of “balanced antagonism” (Kusari et al. 2012). Balanced adaptation between host and endophyte is maintained by avoiding activation of host defense, activation, and production of toxic metabolites by host. On the other hand, if plant defense becomes

strawberry tree (A. unedo)

Mahonia fortunei

Artemisia argyi

Artemisia argyi

Talaromyces pinophilus

Pleosporales sp.F46 &Bacillus wiedmannii Com1

Trichoderma koningiopsis QA-3,

Trichoderma koningiopsis QA-3,

Burkholderia stabilis Panax ginseng EB159 (PG159) Meyer

Picea glauca

Phialocephala scopiformis

Pyrrolnitrin

Vinale et al. (2017)

Sumarah and Miller (2009)

Zhou et al. (2014)

Taechowisan et al. (2006)

Tawfike et al. (2019)

Aboobaker et al. (2019)

Chen et al. (2019)

Reference

Aquatic pathogen Vibrio alginolyticus

Cylindrocarpon destructans

(continued)

Kim et al. (2020)

Shi et al. (2020)

Shi et al. (2020)

Staphylococcus aureus, Wang et al. Bacillus subtilis, Pseudomonas (2019) aeruginosa and Escherichia coli

Acyrthosiphon pisum

Choristoneura Fumiferana & Lambdina fiscellaria

14-hydroxykoninginin E, koninginin U and 14-ketokoninginin B Ceratobasidium cornigerum QDAU-8

15-hydroxy-1,4,5,6-tetra-epi-koninginin G

23R-hydroxy-(20Z,24R)-ergosta-4,6,8(14),20(22)-tetraen-3-one and (22E,24R)-ergosta-4,6,8(14),22-tetraen-3-one

3-O-methyl-funicone

Yellow pigment rugulosin

Antioxidant activity

Alpinia oxyphylla

Streptomyces sp.

2,6-dimethoxy terephthalic acid and yangjinhualine A

Antiinflammatory agents

5,7-dimethyloxy-4-p-methoxylphenylcoumarin and 5,7-dimethoxy-4-phenylcoumarin

S. aureus and E. coli

Alpinia galanga

Dibutyl phthalate (antimicrobial activity)

Aspergillus flavus

Target cells/microorganism

Streptomyces aureofaciens

Pelargonium sidoides root

Penicillium skrjabinii

Phosphate solubilization, siderophore production

Bioactive compounds

Anticancer and antitrypanosomal

Peanut (Arachis hypogaea L.)

Bacillus velezensis LDO2

Aspergillus flocculus Markhamia platycalyx stem

Host plant

Endophyte species

Table 6.2 Endophytes in plant life: action and significance

128 A. Ghasemnezhad et al.

Host plant

Phlegmariurus taxifolius

Polyalthia debilis (Pierre)

Quercus macranthera

Endophyte species

Fusarium sp.

Trichoderma polyalthiae

Neurospora udagawae

Table 6.2 (continued)

Staphylococcus aureus, Macabeo et al. Rhodoturula (2020) glutinisandcytotoxicity against KB3.1 cells

Udagawanones A and B (new α-pyrone)

Cruz-Miranda et al. (2020)

Reference

Staphylococcus saprophyticus, Nuankeaw Staphylococcus aureus, et al. (2020) Methicillin-Resistant S. aureus, Bacillus subtilis, Bacillus cereus, Salmonella typhimurium, Shigella sonnei, and Candida albicans

Treatment of Alzheimer disease

Target cells/microorganism

Violaceol I and II

Huperzine A

Bioactive compounds

6 Microbial Endophytes: New Direction to Natural Sources 129

130 Table 6.3 Endophyte classification

A. Ghasemnezhad et al. Non-clavicipitaceous (NC)

Clavicipitaceous (C)

Fusarium Colletotrichum Phomopsis Xylaria

Atkinsonella Balansia Balansiopsis Echinodothis Epichloe Myriogenospora Neotyphodium Parepichloe

active and fights with fungal agents, the fungus will not be able to colonize plant tissues (De Silva et al. 2019; Kusari et al. 2012; Suryanarayanan et al. 2016). Further, plants produce an array of secondary metabolites against weeds and pathogens. As known, fungi and bacteria produce specialized enzymes and secondary metabolites to overcome these plant defense barriers and defend to cause disease, if pathogenic. For example, endophytic fungi produce toxic compounds, while plants produce antifungal metabolites such as condensed tannins (Schulz et al. 1999; Randriamanana et al. 2018). Some endophytes become pathogens when they are influenced by certain intrinsic and environmental factors to express the factors that lead to pathogenesis (Kusari et al. 2012). The above said phenomenon is common due to excessive moisture or nutrient deficiencies that alter the susceptibility of the host to the natural conditions (De Silva et al. 2019; Fisher and Petrini 1992). Endophyte, such as Epichloe festucae express the mitogen-activated protein kinase (sakA) gene to maintain interaction with the host Lolium perenne (perennial ryegrass). If the fungus is unable to express the gene, the endophyte becomes pathogenic and or disadvantaged in environmental conditions (De Silva et al. 2016). It has recently been observed that gene conferring secondary metabolite production in fungi is non-expressible in pure culture and can be activated in dual experiments with antagonist microbes (De Silva et al. 2019). Fungi act as stimulator for host defense via two mechanisms: (i) acquired systemic resistance (SAR) and (ii) inducible systemic resistance (ISR) (De Silva et al. 2019; Busby et al. 2016). Other various mechanisms of antagonistic activity of an BCA have been described as mycoparasitism, lytic and/or antibiotic production, induction of plant defense, and competition for nutrients and ecological niches (De Silva et al. 2019; Busby et al. 2016). Plant defense responses include altering the biochemistry of cell wall, producing pathogenesis-related proteins (PR), and/or generating specific resistance ISR. In natural conditions, BCAs must tolerate a wider range of climatic factors (temperature, humidity, UV light), soil (soil type), and biotic agents (antagonists), that are not ruling-out under laboratory conditions (Chow et al. 2019). As a result, the levels of defense enzymes are unlikely remain stable at elevated levels and are likely to decrease after several hours or days (Chow et al. 2019). Evidence suggests that endophyte colonization reproduces plant gene expression, reducing physiological

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and biological stresses, improving plant nitrogen utilization, and altering host development (Chow et al. 2019, Dupont et al. 2015). However, the underlying mechanisms of interaction between endophyte BCA, host plant, and pathogen at the transcriptional level remain largely unknown (Chow et al. 2019). Consequently, plant–endophyte interaction involves complex and precise controlled interactions that balance host defense, fungal virulence, and production of secondary metabolites (De Silva et al. 2019) (Table 6.4). Table 6.4 Plant defense responses in relation to endophyte-pathogen and host plant Endophyte kind of endophyte

Biological effect

Results

References

Epichloe festucae

Activation of stress induced protein kinases

Resistance against stress

De Silva et al. (2019)

Endophyte

Lytic and/or antibiotic enzymes

Resistance against stress and diseases

De Silva et al. (2019)

Endophyte

Cell wall alteration, production of proteins associated with pathogenesis (PR) and/or specific resistance (ISR)

Balancing inappropriate plant conditions

De Silva et al. (2019)

endophytic rhizobacteria

Changes in Resistance against plantphysiological stress droughttolerance mechanisms, up-regulation of specific abiotic stress responsivegenes

Govindasamy et al. (2020)

Trichoderma asperellum T1 Productionof volatile antifungal compounds

Antifungal activity against leaf spot fungi C. cassiicola and C. aeria, inducing defense response, and promoting plant growth

Wonglom et al. (2020)

Colletotrichum tropicale

Inducing the expression of Greater plant hundreds of host immunity defense-related genes

Mejía et al. (2014)

Arthrobacter agilis UMCV2

Emission of dimethylhexadecylamine, a volatile compound that induces plant iron uptake mechanisms

Promoting plant growth

Aviles-Garcia et al. (2016)

Bacillus sp.TP1LA1B and Pantoea sp. AP1SA1

Production of phytohormones, siderophores, and organic acids

Improve plant growth and overall fitness

Purushotham et al. (2020)

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6.5 Plant Growth Stimulating Endophytic Bacteria Even, Dharni et al. (2014) and Ma et al. (2016) noted that it is known that PGPB participates in plant growth-promotion and heavy-metal phytoremediation. Various workers resumed that there is little knowledge about plant endophytic bacteria interactions and their potential role in phytoremediation (He et al. 2013; Chen et al. 2014; Babu et al. 2015; Ma et al. 2015). Phetcharat and Duangpaeng (2012) named these bacteria as plant growth-promoting endophytic (PGPE) bacteria and suggested the role of internal colonization for plant-propagation, enhancement of soil fertility, and stimulation of host plant growth by plant growth regulators production. It also has been demonstrated by Ma et al. (2011) that endophytic bacteria may help host plants to adapt under unfavorable environmental conditions and increase the phytoremediation efficiency, promoting the plant growth, alleviating the metal stress, reducing metal phytotoxicity, and finally altering the metal bioavailability and translocation inside the plants. Plant growth-promoting bacteria are a broad group of bacteria that are present in the soil rhizosphere and enter into root-cells and tissues under complex signaling mechanisms. A group of these bacteria called ‘endophyte–s’ which are able to reach toward plant host using chemotaxis, and enter into plant tissues through the lenticels, wounds caused by trichome breaks, stomata, exit zone of lateral roots and the area of root radical (Hallmann et al. 1997; 1998). These microorganisms grow in the apoplast or simplest space of plant root tissues without causing obvious damage (Gimenez et al. 2007). They often proliferate in the intercellular space of the root or may enter the peripheral circular cells. These develop systemic-infection and enter into parenchymal cells (Hallmann et al. 1997; 1998). Specific genetic systems are then activated between the bacterium and plant (Hardoim et al. 2008). The above symbiotic bacteria provide various benefits, such as increased level of resistance to stress and improvement of plant growth conditions (Dheeman et al. 2017). This relationship provides a balance between the plant and endophyte, but if environmental conditions are manipulated in favor of endophyte, the endophyte becomes pathogenic to disturb homeostasis drastically (Aly et al. 2010). There are various ways by which bacterial endophytes can confer resistance or tolerance to the host plant from different biotic and abiotic stresses (Santoyo et al. 2016). Endophytic bacteria utilize the nutrients, assimilated in plants and stabilizing nitrogen in-turn. These are also involved in production of 2-, 3-butanol, and acetone (Sturz et al. 2000), as well as secreting hormones such as ethylene, auxin, cytokinin, gibberellin, etc. By the production of terpenoids, flavonoids, isoflavonoids they help plant in developing resistance against pathogens and counter-acting environmental stresses. In addition to these, endophytic bacteria produce antifungal compounds, i.e., siderophore, which enhance iron-absorption, competition for food, limiting ecological-niche, and favoring plant-resistance mechanisms. Hence, it is worthy to understand that, PGPR is an important player of biological control (Hardoim et al. 2008; Jha et al. 2013). Research on Chinese medicinal plant Ferula songorica revealed that this plant is a rich reservoir of endophytic bacteria with an ability to solubilize phosphate and producing enzymes such as protease and cellulose (Yadav

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et al. 2020). In the endophytic relationship, microbes provide a unique opportunity indirectly for control of the deleterious impact of phytopathogens on health of plant and soil, via synthesis of innumerable compounds, for example, antibiotics, immunesuppressants, biocontrol agents, hydrogen cyanide (HCN), and ammonia, induced systemic tolerance, production of hydrolytic enzymes (Yadav et al. 2017). In addition, few endophytic bacteria are also used in genetic engineering to transfer specific genes to the host plant (Tomasino et al. 1995). Endophytic microbes can maintain sustainable agriculture, i.e., enhanced the health, yield, productivity of plants via numerous independent or linked mechanisms. There are many reports on isolation of endophytic bacteria from roots, stems, leaves, seeds, needles, twigs, and barks of different plant species and their agricultural applications (Yadav et al. 2020). Nitrogen-fixing endophytes make up a small portion of the total population of endophytes and they are mainly considered for nitrogen fixation. Nitrogen-fixing endophytes have been found in seed and root of some rice cultivars (Mano and Morisaki 2008). Recently, more focus is laid on the isolation and identification of nitrogen-fixing endophytic bacteria in cereal crops (Verma et al. 2015, 2019).

6.6 Biodiversity of Bacterial Endophytes Previous reviews have described the diversity of bacterial endophytes in multiple plant species, especially those with agronomical interest (Rosenblueth and MartínezRomero 2006). More recently, Romero et al. (2014) demonstrated the power of the 16S-rRNA pyrosequencing approach in determining the position of endophytic bacterial communities in tomato. The endophyte communities were mainly comprised of five phyla, with Proteobacteria as the most highly represented as 90%. Other phyla detected were actinobacteria by 1.5%, Planctomycetes 1.4%, Verrucomicrobia 1.1%, and Actinobacteria is only about 0.5%. In addition, the dynamics of endophytic bacterial communities of sugar beet (Beta vulgaris L.) with different plant genotypes and plant growth stage changes was recently analyzed by PCR-based llumina pyrosequencing (Shi et al. 2014). The most abundant division was the Proteobacteria, with 98% of the total microbial endophyte community being composed of Enterobacteriales, Pseudomonadales, Xanthomonadales, Rhizobiales, Sphingomonadales, Burkholderiales, Actinomycetales, and flavobacteriales. In general, the Phylum Proteobacteria, including the classes α, β, and γ -Proteobacteria, are reported to be dominant in diversity analysis of endophytes. Although, members of the Firmicutes and Actinobacteria are also among this classes as most consistently found as endophytes. Other classes such as Bacteroidetes, Planctomycetes, Verrucomicrobia, and Acidobacteria are less commonly found as endophytes. The most commonly found genera of bacterial endophytes are Pseudomonas, Bacillus, Burkholderia, Stenotrophomonas, Micrococcus, Pantoea, and Microbacterium (Romero et al. 2014; Rosenblueth and Martínez-Romero 2006; MarquezSantacruz et al. 2010; Shi et al. 2014). All these genera, described as bacterial

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endophytes, are also common inhabitants of the rhizosphere. Therefore, it has been suggested that the endophyte microbiome may be a sub-population of the rhizosphere inhabiting bacteria (Marquez-Santacruz et al. 2010). The genus Pseudomonas is ubiquitous in nature and part of the core endo-microbiome of many plants ranging from model plants like Arabidopsis thaliana to medicinal plants like Cannabis sativa. Pseudomonas sp. can confer unique characteristics to the host plant and are well known for plant (Purushotham et al. 2020). More than 300 endophytic actinobacteria and bacteria belonging to the genera Streptomyces, Nocardiopsis, Brevibacterium, Microbacterium, Tsukamurella, Arthrobacter, Brachybacterium, Nocardia, Rhodococcus, Kocuria, Nocardioides, Pseudonocardia etc., were isolated from different tissues of Dracaena cochinchinensis Lour. (a traditional Chinese medicine known as dragon’s blood). Of these, 17 strains having antimicrobial and anthracyclines-producing activities also showed antifungal and cytotoxic activities against two human cancer cell lines, MCF-7 and Hep G2 (Salam et al. 2017). The majority of endophytic bacteria produce different kinds of antibiotics. Ecomycin, pseudomycins, and kakadumycins are some of the novel antibiotics produced by endophytic bacteria (Christina et al. 2013).

6.7 Interactions of Endophytes and the Host Plant Importantly, similar to any other living organism, plants are flexible and can adapt themselves and integrate with a different environment by strategically facing external stresses. For instance, the healthy growth and complex adaptive response of plants, often categorized as an intelligent response by a few authors (Chamovitz 2018), is associated with this world of microbes. It is intriguing to note that even after 500 million years of evolution, plants still need the assistance of the endophytic community to be able to resist stress tolerance including climate change and adapt themselves to their continuously changing environments (Deng and Cao 2017). This adaptation behavior is directly buttressed by the production of bioactive compounds known as secondary metabolites (Singh 2019). The endophytes survive on the nutrients produced by the plants and in return, these endophytes yield functional metabolites for their host plants. There is a positive linear relationship between endophytes and their host plants in terms of the production of these bioactive compounds (Palanichamy et al. 2018). Since endophytic fungal elicitors belong to extracellular materials and cannot directly enter the cell to play a role, the process of endophytic fungal elicitors to influence the secondary metabolism of plant cells through signal pathways will first identify and bind to the plant specific receptors on the cell membrane, change the structure of the cell to promote the production of specialized intracellular messenger substances. These messenger substances can regulate the expression of related genes in the nucleus through a series of signal transduction pathways. Finally, the defensive secondary metabolic system is activated, and the synthesis of secondary metabolites (Yan et al. 2020). Hernández-Soberano et al.

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(2020) described Arthrobacter agilis UMCV2 and Bacillus methylotrophicus M496 as bacteria that stimulate plant growth in vitro. A. agilis UMCV2 behaves as an endophytic bacterium of Medicago truncatula (Aviles-Garcia et al. 2016) and promotes plant growth by emission of dimethylhexadecylamine, a volatile compound that induces plant iron uptake mechanisms and systemic resistance (Raya-González et al. 2017), and modulates plant morphogenesis (Castulo-Rubio et al. 2015; VázquezChimalhua et al. 2019). B. methylotrophicus M4-96 promotes growth in Arabidopsis and strawberries by emission of the phytostimulant volatile compound acetoin, and the production of the plant growth regulators (PGR), indole acetic acid and gibberellic acid (Pérez-Flores et al. 2017; Vicente-Hernández et al. 2019). Because, endophytes reside within plants and are continuously interacting with their hosts, it is conceivable that plants would have a substantial influence on the in planta metabolic processes of the endophytes. For example plants homoserine and asparagine act as host signals to activate expression of a lethal gene in virulent strains of Nectria hematococca that is only expressed in planta. Furthermore, expression of the gene cluster for lolitrem biogenesis in endophytic Neotyphodium lolii resident in perennial ryegrass is high in planta, but low to undetectable in fungal cultures grown in vitro, lending support to the notion that plant signaling is required to induce expression (Young et al. 2006). Another convincing example is that of the symbiotic association between dicotyledonous plants (Convolvulaceae) and clavicipitaceous fungi leading to synthesis of ergoline alkaloids by the fungus, and question the origin of these compounds in plants (Leistner and Steiner 2009). Recently, it was found that a camptothecin-producing endophyte, F. solani isolated from C. acuminata, could indigenously produce the precursors of camptothecin. However, a host plant enzyme absent in the fungus, strictosidine synthase, was employed in planta for the key step in producing camptothecin. This was the main reason for substantial reduction of camptothecin production on subculturing under axenic conditions. Such plant-fungus interactions compel reconsidering whether horizontal gene transfer (plant to endophyte genome or vice versa) is the only mechanism by virtue of which endophytes produce associated plant compounds (Kusari et al. 2012). The production of natural products by endophytic fungi, once considered exclusive to plants, also raises intriguing questions regarding the original source organism. Actually, it is possible that various so-called ‘plant metabolites’ could in fact be the biosynthetic products of their endophytes. An important example is the production of the very potent antitumor maytansinoid ansamitocin, originally isolated from higher plants, by the actinobacteria Actinosynnema pretiosum ssp. auranticum (Yu et al. 2002). This study substantiated the possibility that the true biosynthetic source of the maytansinoid backbone could be a bacterial endophyte. Although, horizontal gene transfer may explain the production of maytansinoids by plants, a more likely scenario is the production of maytansinoids by symbionts. Because, the interaction between endophytic fungi with the host plant and other endophytes remains versatile, even slight variations in the in vitro cultivation conditions can impact the kind and range of secondary metabolites they produce. It is well established that the metabolic processes of microorganisms are critically dependent on the culture parameters. This is especially exemplified by endophytes because their range of interactions is so

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broad. For example, the plant associated Paraphaeosphaeria quadriseptata starts producing six new secondary metabolites when only the water used to make the media is changed from tap water to distilled water (Kusari et al. 2012).

6.8 Endophytes and Abiotic Stresses Human activities such as smelting, mining, electroplating, refineries, fertilizer use and fungicides, sewage sludge have accumulated heavy metals such as cadmium (Cd) in natural resources, soil and climate. The accumulation of Cd in plants causes severe damage to the cell membrane, organelle and nucleus as a result of reduced metabolism, photosynthesis and absorption of water and nutrients. In addition, Cd enrichment in crops can pose a risk to human health (Tang et al. 2019). Recently, studies on plant growth-promoting endophytes have shown the potential role of selected endophytes for improving plant growth, development and mineral uptake, and resistance to stress under harsh environmental conditions (Tang et al. 2019) (Fig. 6.3). The Acinetobacter guillouiae EU-B2RT.R1 with multifarious plant growthpromoting activity has emerged as one of the efficient biofertilizers that need to be explored for sustainable agriculture (Rana et al. 2020). Li et al. (2007) reported that Gram-negative Burkholderia cepacia increased biomass, metal uptake, and tolerance index in S. alfredii. Xinxian et al. (2011) isolated 14 endophytic strains from S. alfredii roots and demonstrated that stimulatory activity of plant growth was associated with heavy metal accumulation in different plant organs in response to metal stress. Similar results with B. juncea (Belimov et al. 2005), Salix caprea L. (Kuffner et al. 2008), and H. Annus (Kolbas et al. 2015) were obtained. Similarly K. rhizophila has been reported as a bio-sorbent for cadmium (Cd) and chromium (Cr) and can remove metal ions from aqueous solutions. Metal-resistant bacteria increase plant growth and accumulation of heavy metals in plant organisms in association with application (EDTA) (Afridi et al. 2019) (Table 6.5).

Fig. 6.3 Positive effect of endophyte coexistence with poplar seedlings (Khan et al. 2016)

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Table 6.5 Endophytes and abiotic stresses Endophyte

Biological role

References

Burkholderia cepacia

Increasing biomass, metal uptake, and tolerance index

Li et al. (2007)

K. rhizophila

Inducing the uptake of Cd and Cr Afridi et al. (2019)

Bacillus pumilus

Improving salinity tolerance and Khan et al. (2016a, b) alleviating heavy metals toxicity

Bacillus pumilus

Enhancing drought stress resistance

Xie et al. (2019)

Scenedesmus obliquus, Euglena Detoxification of DDT, parathion Ardal (2014) gracilis Chlamydomonas sp.

Detoxification of Lindane, naphthalene, phenol

Bacillus cereus strain XMCr-6

Alleviating heavy metals toxicity Dong et al. (2013) (Cr)

Aspergillus fumigatus

Alleviating heavy metals toxicity Kumar et al. (2011) (Pb)

Acinetobacter calcoaceticus

Nitrogenase activity and enhancing the capability of growing under nitrogen-limited conditions

Doty et al. (2009)

Pantoea alhagi

Improving growth and drought tolerance

Chen et al. (2017)

Acinetobacter guillouiae EUB2RT. R1

Increasing biomass, enhancing Fe and Zn content

Rana et al. (2020)

Epichloe gansuensis

tolerate physiological conditions Ahmad et al. (2020) i.e. salinity, pH, temperature, photoperiod and light variation

Calvibacter sp.

Improving chilling tolerance

Ding et al. (2011)

Group strains of Bacillus, Microbacterium, and Halomonas

Biodegradation Textile effluent

Wang et al. (2017)

Bacillus thuringiensis GDB-1

Alleviating heavy metals toxicity Wang et al. (2018) (As, Cu, Pb, Ni, and Zn)

Aspergillus sp. A31, C. geniculata P1, Lindgomycetaceae P87 and Westerdykella sp. P71

Mercury resistance and bioremediation

Pietro-Souza et al. (2020)

Other studies of endophyte–plant cooperation in stressful conditions reveal good results. For example, endophytes help pepper plants tolerate nitrogen deficiency conditions (Fig. 6.4). In other studies, resistant endophyte species were detected in the seeds of C4 and CAM plants from resistant strains of C4 and CAM plants of the phylum Firmicutes. These bacteria are known to be involved in the thermal

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Fig. 6.4 Comparison of un-inoculated and endophyte-inoculated pepper plants under nitrogen deficiency conditions (Khan et al. 2012)

regulation and protection of plants through enzymes, antibiotic synthesis, and strong adaptation to C4 and CAM plants (Girsowicz et al. 2019). Plant growth-promoting bacteria (PGPB), a type of endophyte bacteria, are extremely capable of adjusting physiological responses to water deficiency, which ensures plant survival in stressful conditions. Bacillus pumilus is an important PGPB that plays a key role in improving salt-tolerance of rice (Khan et al. 2016b) and alleviating metal toxicity in tomatoes (Khan et al. 2016a). Drought stress resistance of Glycyrrhiza uralensis (Fisch) was improved by B. pumilus, possibly through increased activity of antioxidant enzymes and improved synthesis of glycyrrhizic acid, which is associated with the expression of proteins like HMGR, SQS, and β-AS (Xie et al. 2019). Colonization of B. amyloliquefaciens SB9 was also able to counteract the adverse effect of salt and drought-induced stresses by reducing the production of malondialdehyde (MDA) and reactive oxygen species (ROS) in grape-wine roots (Jiao et al. 2016). There have been a large number of studies (Glick 2010, 2014; BecerraCastro et al. 2013; Sessitsch et al. 2013; Muehe et al. 2015) indicating that plantassociated microorganisms are indeed essential players in metal phytoextraction or phytomining, enhancing the plant growth and health by the increase of nutrient uptake and improving their resistance to pathogens and stress (Lugtenberg and Kamilova 2009). It is known that most of the phosphate-solubilizing bacteria and siderophore producers, bacteria with ACC deaminase activity and phytohormone producers, improve plants’ growth and transform heavy metals into soluble and bioavailable forms, favoring that plants take up contaminants (Ullah et al. 2015; Guerrero-Zúñiga et al. 2020). Thus, these kinds of bacteria can assist in the phytoremediation of heavy metals, either directly or indirectly: directly involving the solubilization and removal of them from solid matrices, such as soil, dumps, sediments, and other industrial and municipal wastes, giving more bioavailability and final accumulation by plants, and indirectly, by the improvement of plants’ growth to prevent the

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effect of phytopathogens, facilitating the accumulation of heavy metals (Glick 2010; Guerrero-Zúñiga et al. 2020).

6.9 Antimicrobial Activity of Endophytes Endophytes are recognized as valuable sources of biologically active secondary metabolites and various structures. However, most of their gene clusters are still silent, indicating a greater biosynthetic potential for the production of diverse metabolites. Several methods have been developed to activate biosynthetically silent gene clusters in order to produce hidden natural products. One of them is co-cultivation that is recognized as a powerful way to enhance chemical diversity. A reason why the structural diversity of natural products is expanding is the interspecific interference among microorganisms, especially those that reside in a similar ecological environment (Wang et al. 2019). Trait propagation, e.g., antibiotic production, through activating biosynthetically silent gene clusters is typically associated with interspecific interference. Wang et al. (2019) isolated, detected, and biologically assessed a new derivative of ergosterol (23R-hydroxy-(20Z,24R)-ergosta-4,6,8(14),20(22)tetraen3-one) and a biosynthetically known compound from the co-cultivation of the endophytic fungus Pleosporales sp. F46 and the endophytic bacterium Bacillus wiedmannii sp., both residing in the medicinal plant Mahonia fortune. This is the first ergosterol derivative with a double Z20 bond in the side chain and shows strong antibacterial activity. Peanut endophyte Bacillus velezensis LDO2 is highly capable of synthesizing various antimicrobial metabolites and shows strong antagonistic activities against fungal and bacterial pathogens of peanut. The gene clusters responsible for their antifungal metabolites (fengycin, surfactin, and bacilysin) and antibacterial metabolites (butirosin, bacillaene, difficidin, macrolactin, surfactin, bacilysin) were detected (Chen et al. 2019). Li et al. (2016) investigated the antifungal activity of crude extracts of 93 endophytic fungi, isolated from five kinds of tissues of Zanthoxylum bungeanum on F. sambucinum and P. zanthoxyli. Another study on strawberry plants revealed that the soil application of endophyte in the strawberry medium improved growth conditions and viability of the plants significantly (Fig. 6.5). Aboobaker et al. (2019) were the first to report Penicillium skrjabinii as an endophyte that synthesizes dibutyl phthalate. This compound contributes to endophytic– host plant interactions and has an antimicrobial effect against S. aureus and E. coli. Fructose and peptone are the best sources of carbon and nitrogen for the production of most antimicrobial metabolites of PG159. Biological metabolites synthesized by bacteria are generally regarded as bio-pesticides. Bacterial metabolites contain bioactive compounds with antagonistic activities such as pyrrolnitrin, phenazine, cepabactin, and other unknown compounds. Pyrrolnitrin is produced as a fungicide against soil-borne fungal pathogens, such as Rhizoctonia solani that is the cause of seedling death (Kim et al. 2019). Cui et al. (2020) reported that the healthy potatoes can carry endophytic bacterium which have the antagonistic ability against potato

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Fig. 6.5 The effect of the fungus Beauveria bassiana as an endophyte on strawberries (Dara and Dara 2015)

diseases. The antagonistic bacteria B. velezensis strain 8-4 could control not only potato scab, but also potato anthracnose, gangrene, blight, and black shank as a broad-spectrum antagonistic agent with potential applications in the disease control (Cui et al. 2020). Worldwide, powdery mildew (PM) is a common disease of plants caused by obligate biotrophic fungal pathogens (Liang et al. 2018). Bacillus spp. have been found to be effective biocontrol agents of PM (Panstruga and Kuhn 2019). Jakuschkin et al. (2016) also found that endophytes Mycosphaerella punctiformis and Monochaetia kansensis have antagonistic activities against oak PM. Clark et al. (2014) reported that the extract of Seimatosporium sp. isolated from the Canadian medicinal plant Hypericum perforatum exhibited better antifungal and antimycobacterial activity. Spry et al. (2018) also found that the fermentation broth of Seimatosporium sp. CL28611 displayed excellent anti-plasmodial activity in vitro. Zhao et al. (2020) reported that the isolate Seimatosporium sp. M7SB 41 from the PM resistance Rosa variety may play an important role in host plant PM resistance through producing some antimicrobial metabolites.

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6.10 Endophytic Bioactive Alkaloids Endophytes are an active source of bioactive alkaloids that protect their host plants. The positive effect of Epichloë endophytes on plant defense has been traditionally attributed to fungal alkaloids. Alkaloids are nitrogen-rich compounds, four groups of which have been detected in endophytes: ergot alkaloids (e.g., ergopeptine and ergovaline), indole-diterpene (e.g., lolitrem B and epoxy-janthitrem), pyrrolizidine (e.g., lolines), and pramine. All enzymes involved in their synthesis are encoded in the fungal genome and all biosynthetic pathways are mainly defined. Alkaloid profiles depend on the species and strain of endophyte and the amount of alkaloids is related to plant phenological stage, plant tissue, and environmental conditions. In addition, the effectiveness of an alkaloid defense against an invader depends on the concentration and chemical type of the alkaloid produced by the endophyte (Bastias et al. 2017). Endophytic Bacillus cereus, Aranicola proteolyticus, Serratia liquefaciens, Bacillus thuringiensis, and Bacillus licheniformis isolated from Pinellia ternata have the ability to produce alkaloids (guanosine and inosine) in fermentation broth similar to their host plant (Liu et al. 2015). The capsular endophyte Acinetobacter SB1B in Opium poppy unregulated the expression of key genes for the benzylisoquinoline alkaloid (BIA) biosynthesis except thebaine and codeine. In contrast, Marmoricola sp. SM3B, another endophyte, could up-regulate the biosynthesis of both thebaine and codeine. Acinetobacter and Marmoricola sp. as microbial inoculants modulated the alkaloid producing genes in Opium poppy (Pandey et al. 2016). The impairment of the cholinergic neurotransmission in the central nervous system is one of the bases of memory deficit related to Alzheimer’s disease (AD), with the administration of acetylcholinesterase (AChE) inhibitors representing the most acceptable strategy for treating this illness. Huperzine A (Hup A) is an alkaloid, which was first isolated from the Chinese Huperzia serrata (Thunb. ex Murray) Trev., and gained attention due to its potent, reversible, and selective inhibition of AChE. Furthermore, the molecule penetrates the hemato-encephalic barrier more effectively, has greater oral bioavailability and the AChE inhibitory action lasts longer than other commercial drugs (donepezil and rivastigmine) (wang et al. 2006; Cruz-Miranda et al. 2020). For this reason, in the last few years, there is an increased interest in the discovery of a microbial source with the potential to produce Hup A. Some reports have described fungal endophytes that were isolated from different species of lycophytes producing Hup A. The fungi Shiraira sp. SIf14, Cladosporium cladosporioides, and Colletotrichum gloeosporioides ES026 were isolated from H. serrata (Shu et al. 2014), whereas the endophytic fungi Ceriporialacerata and Hypoxylon investiens were isolated from Phlegmariurus phlegmaria (Zhang et al. 2015; Cruz-Miranda et al. 2020). Some endophytic fungi can produce the same bioactive compounds as their host plants, e.g., camptothecin, hypericin, vinblastine, paclitaxel, podophyllotoxin, and diosgenin. For example, Taxomyces andreanae is an endophytic fungus isolated from the Taxus brevifolia tree and has the potential to produce the anticancer compound Taxol. In addition, endophytic fungi can produce the antidepressant hypericin and

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Table 6.6 Some endophyte fungi as a medicinal source Endophyte

Medicinal compound

References

Cylindrocarpon lucidum

Immunosuppressant cyclosporine

Abdel-Azeem et al. (2019)

Tolypocladium inflatum

Immunosuppressant cyclosporine

Abdel-Azeem et al. (2019)

Aspergillus terreus

Lovastatin

Abdel-Azeem et al. (2019)

Penicillium sp.

Antibiotic penicillin

Abdel-Azeem et al. (2019)

Chaetomium globosum

Anti-rheumatoid activity

Abdel-Azeem et al. (2016)

Taxomyces andreanae

Taxol

Stierle et al. (1993)

Acremonium sp.

Paclitaxel (Taxol)

El-Bialy and El-Bastawisy (2020)

Pestalotiopsis microspora

Paclitaxel (Taxol)

Kusari et al. (2014)

Fusarium solani

Camptothecin (topoisomerase inhibitor)

Kusari et al. (2012)

Actinomycete Actinosynnema pretiosum ssp. auranticum

Maytansinoid ansamitocin

Yu et al. (2002)

Diaporthe sp.

Diaporone A (new dihydroisocoumarin), α-dibenzopyrones

Guo et al. (2020)

Fusarium sp.

Huperzine A

Cruz-Miranda et al. (2020)

Ceriporia lacerata

Huperzine A

Zhang et al. (2015)

Trichoderma polyalthiae

Violaceol I and II

Nuankeaw et al. (2020)

B. amyloliquefaciens SB-9

Melatonin

Jiao et al. (2016)

Streptomyces Strain MS-6-6

Treponemycin (Anti-tuberculous)

Mahmoud et al. (2015)

Streptomyces sp. MK932-CF8

Androprostamines (Anti-prostate cancer)

Yamazaki et al. (2015)

Pseudomonas syringae

Pseudomycin

McEvoy et al. (2016)

emodin, deoxypodophyllotoxin, antineoplastic camptothecin (CPT), as well as the natural insecticides azadirachtin A and B (Table 6.6).

6.11 Endophytes in Agriculture and Medicine: Future Prospects Since the emergence of mankind, plants have always been a major nutritional source, along with animals, for us so that they have been used as a source of food and treatment. Today, given the industrial development and population growth in most countries, land fragmentation into small parcels has reduced farmlands and crop

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production, which has had negative impacts in the face of population growth. As such, the application of proper and optimal management practices for the efficient use of lands has drawn the attention of scientific circles. On the other hand, it can be useful to apply methods that can improve production efficiency. Producers are always concerned about the limiting factors of crop production, e.g., adverse climatic and nutritional conditions, pathogens, and spatial limitations. As already described, endophytes are bacteria or fungi that penetrate a plant and influence it positively without creating disease symptoms (although they may turn out to be pathogenic in some unfavorable growth conditions) (Wilson 1995). In this regard, it is important and practical to understand endophytes, their relationships with their host, and their various ecological and nutritional needs (Nair and Padmavathy 2014). Since endophytes can be present in different parts of a plant, this is an advantage for us as we will not be restricted in their application (Pirttilä et al. 2000, 2003). In the first place, various studies have been carried out on endophyte symbiosis with plants in agriculture, suggesting different ways to isolate endophytes (Hallmann et al. 1997; Reinhold-Hurek and Hurek 1998). It is important to answer the questions as to how to extract endophytes, how to cultivate them, and where to cultivate them to obtain them in great deals. This encompasses different environments, research on which is underway and should be expanded in the future (Rai et al. 2007; Hata and Sone 2008). Based on the research already conducted, some endophytes can be applied in production processes (Table 6.7). Today, given the change of climates in the world and the diversity of agricultural production sites, the climatic conditions should always be considered (Nair and Padmavathy 2014). For example, a study showed that changes in climatic conditions and the resulting changes in plant size may affect endophyte abundance (Rai et al. 2007; Chareprasert et al. 2006). In this light, future research should focus on the ecological requirements of endophytes to figure out the optimal conditions for the individual endophytes. Research on endophytes has been undertaken in a variety of fields, and environmental conditions should be properly assessed to obtain better results. Given the modern advances in biotechnology, endophytes can be presented as an important and useful tool. Diverse studies have addressed using endophytes as molecular markers and transporter genes. In addition to these roles, their beneficial side effects can be utilized for the benefit of the plants (Dheeman et al. 2017). The technology needs developments in the consideration of science expansion and well-being of humans (Nair and Padmavathy 2014; Araujo et al. 2002). It is known that plants need a wide range of elements for survival and the deficiency of any of these elements can influence their growth and production negatively. Some important agriculture-related measures can be enumerated as endophytes in nutrient uptake, balanced establishment, stress-free conditions for plants, and production of secondary metabolites those are not just limited to farming but also expanded into other biological fields, like in biological control, organic farming, antimicrobial compound, synthesis of important enzymes, and in tissue culture as major tool in agriculture (Nair and Padmavathy 2014). Overall, endophytes can be considered as plant contributors, their roles are not limited to a single field but encompass various sequential fields. On the other hand, with respect to the close relationship of medical

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Table 6.7 Some fungi used as endophytes in different plants (Nair and Padmavathy 2014) Endophytes

Plant species

References

Phomopsis sp.

Neolitsea sericea

Santangelo et al. (2015)

Pasania edulis

Arnold et al. (2003)

Ginkgo biloba L.

Mano and Morisaki (2008)

Tectona grandis and Samanea saman Merr.

Tomasino et al. (1995)

Taxus chinensis

Stone et al. (2000)

Cladosporium sp.

Opuntia ficus indica

Hallmann et al. (1998)

Cinnamomum camphora

Zhao et al. (2010)

C. herbarum

Lycopersicum esculentum Mill.

Pirttilä et al. (2003)

Triticum aestivum

Hallmann et al. 1997

Triticum aestivum

Hallmann et al. 1997

Colletotrichum sp.

Citrus plants

Belimov et al. (2005)

Cinnamomum camphora

Zhao et al. (2010)

Pasania edulis

Arnold et al. (2003)

Ginkgo biloba L.

Mano and Morisaki (2008)

Tectona grandis and Samanea saman Merr.

Tomasino et al. (1995)

Huperzia serrate

Porter et al. (1976)

Cinnamomum camphora

Zhao et al. (2010)

C. gloeosporiodes

Lycopersicum esculentum Mill.

Pirttilä et al. (2003)

Phyllosticta sp.

Citrus sp.

Belimov et al. (2005)

Pasania edulis

Arnold et al. (2003)

Coffea Arabica

Reinhold-Hurek and Hurek (1998)

Centella asiatica

Rai et al. (2007)

Panax quinquefolium

Hata and Sone (2008)

Ginkgo biloba L.

Mano and Morisaki (2008)

Lycopersicum esculentum Mill.

Pirttilä et al. (2003)

Huperzia serrate

Porter et al. (1976)

Taxus chinensis

Stone et al. (2000)

Huperzia serrate

Belimov et al. (2005)

Trichoderma koningiopsis QA-3,

Artemisia argyi

Shi et al. (2020)

Fusarium solani

C. acuminata

Kusari et al. (2012)

Diaporthe sp.

Pteroceltis tatarinowii Maxim.

Guo et al. (2020)

Ceriporia lacerata

Phlegmariurus phlegmaria

Zhang et al. (2015)

Aspergillus versicolor strain Eich.5.2.2

Eichhornia crassipes

Ebada and Ebrahim (2020)

Penicillium sp. Acremonium sp.

(continued)

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Table 6.7 (continued) Endophytes

Plant species

References

Bacillus sp. TP1LA1B and Pantoea sp. AP1SA1

Pseudowintera colorata

Purushotham et al. (2020)

science and agriculture, these can supply active and pharmaceutical ingredients for disease prevention and cure, endophytes can be a good topic of research in medical science too. For example, they have a high potential in the production of raw material for drugs as they produce antimicrobial compounds and bioactive compounds that have beneficial pharmacological effects. A reason for the importance of plantderived endophytes is their antimicrobial role, which can be effective in both plants and animals (Sette et al. 2006; Kumar et al. 2011). For example, 18 compounds from Tectona grandis L. and 37 compounds from Samanea saman Merr have antibacterial activities (Chareprasert et al. 2006). In addition, endophytes have biological constituents that can be used in targeted drug delivery. Some of them can also be effective as anticancer and immune enhancer compounds (Joseph and Priya 2011). Some major medicinal compounds (Fig. 6.6), which have been derived from endophytes and have anti-pathogenic and medicinal activities, include Maytansinoids (Pullen et al. 2003), Siderophores, etc. (Neilands 1993), Taxol as an important compound in the treatment of cancers, and Huperzine A (Liu et al. 2009). Acremonium sp. showed the presence of BAPT gene that is responsible for paclitaxel production and encoding C-13 phenylpropanoid side chain-acetyl coenzyme A acetyltransferase. Therefore, the selected endophyte has an individual metabolic system that can be activated in the absence of the host or changing its ecology (El-Bialy and El-Bastawisy 2020). Nuankeaw et al. (2020) showed the broad spectrum of violaceol which had the potential antimicrobial activities against human pathogens. This is the first report of phenol violaceol produced by a species of Trichoderma. Pyrrolnitrin is a broad-spectrum antibiotic produced by many strains of the genera Burkholderia, Pseudomonas, Enterobacter, Acinetobacter, Myxococcus, Serratia

Fig. 6.6 Chemical structures of some bioactive compounds produced by endophytic microorganisms (a) Taxol (b) Huperzine A

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etc. (Mujumdar et al. 2014; Kim et al. 2020). Pyrrolnitrin is also an important antimicrobial agent for plant protection (Dheeman et al. 2017). The mode of action of pyrrolnitrin is not clear, but interference in fungal plasma membranes has been demonstrated. Four genes in chromosomal DNA (6.2-kb region) are responsible for pyrrolnitrin production in Pseudomonas fluorescens, while plasmid-encoded genes are responsible in Acinetobacter haemolyticus A19 (Kim et al. 2020). Endophytic bacterial strain, EML-CAP3 isolated from Capsicum Annum L. (red pepper) leaf, showed potent antiangiogenic activity. This endophytic bacterial strain produced lipophilic peptides which inhibited the proliferation of human umbilical vein endothelial cells and also exhibited antiangiogenic potential in tumor progression (Jung et al. 2015). In general, endophytes have many unsolved mysteries, each of which can add to human knowledge and make it easier for human beings to deal with anomalies in various fields.

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and slows Botrytis cinerea infection by two different methods of interaction. J Plant Growth Regul. https://doi.org/10.1007/s00344-018-9888-6 Vinale F, Nicoletti R, Lacatena F et al (2017) Secondary metabolites from the endophytic fungus Talaromyces pinophilus. Nat Prod Res 31(15):1778–1785 Wang L, Lin H, Dong YB et al (2018) Isolation of vanadiumresistanceendophytic bacterium PRE01 from Pteris vittata in stone coal smelting district and characterization for potential use in phytoremediation. J Hazard Mater 341:1–9 Wang R, Yan H, Tang XC (2006) Progress in studies of huperzine A, a natural cholinesterase inhibitor from Chinese herbal medicine. Acta Pharmacol Sin 27(1):1–26. https://doi.org/10.1111/j.17457254.2006.00255.x Wang YH, Li HH, Feng GJ et al (2017) Biodegradation of diuron by an endophytic fungus Neurospora intermedia DP8-1 isolated from sugarcane and its potential for remediating diuron-contaminated soils. PLoS One 12(8):e0182556 Wang ZR, Li G, Ji LX et al (2019) Induced production of steroids by co-cultivation of two endophytes from Mahonia fortunei. Steroids 145:1–4 Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73(2):274–276. https://doi.org/10.2307/3545919 Wonglom P, Ito SI, Sunpapao A (2020) Volatile organic compounds emitted from endophytic fungus Trichoderma asperellum T1 mediate antifungal activity, defense response and promote plant growth in lettuce (Lactuca sativa). Fungal Ecol 43:100867 Xie Z, Chu Y, Zhang W, Lang D, Zhang X (2019) Bacillus pumilus alleviates drought stress and increases metabolite accumulation in Glycyrrhiza uralensis Fisch. Environ Exp Bot 158:99–106. https://doi.org/10.1016/j.envexpbot.2018.11.021 Xinxian L, Xuemei C, Yagang C, Woon-Chung WJ, Zebin W, Qitang W (2011) Isolation and characterization endophytic bacteria from hyperaccumulator Sedum alfredii Hance and their potential to promote phytoextraction of zinc polluted soil. World J Microbiol Biotechnol 27(5):1197–1207 Yadav AN, Kumar R, Kumar S et al (2017) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5(6):45–57. https://doi.org/10.7324/JABB.2017.50607 Yadav AN, Singh J, Rastegari AA, Yadav N (2020) Plant microbiomes for sustainable agriculture. Springer, Cham Yamazaki Y, Someno T, Igarashi M, Kinoshita N, Hatano M, Kawada M et al (2015) Androprostamines A and B, the new anti-prostate cancer agents produced by Streptomyces sp. MK932-CF8. J Antibiot 68:279–285. https://doi.org/10.1038/ja.2014.135 Yan K, He L, Yang K (2020) Effects of SA and H2 O2 mediated endophytic fungal elicitors on essential oil in suspension cells of Cinnamomum longepaniculatum. Open Acc Lib J 7(1):1–12. https://doi.org/10.4236/oalib.1106009 Young CA, Felitti S, Shields K et al (2006) A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet Biol 43:679–693 Yu TW, Bai L, Clade D et al (2002) The biosynthetic gene cluster of the maytansinoid antitumor agent ansamitocin from Actinosynnema pretiosum. Proc Natl Acad Sci USA 99:7968–7973 Zhang FF, Wang MZ, Zheng YX, Liu HY, Zhang XQ, Wu SS (2015) Isolation and characterization of endophytic huperzine A-producing fungi from Phlegmariurus phlegmaria. Microbiology 84(5):701–709. https://doi.org/10.1134/s0026261715050185 Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23(5):753–771. https://doi.org/10.1039/b609472b Zhao J, Zhou L, Wang J et al (2010) Endophytic fungi for producing bioactive compounds originally from their host plants. Curr Res, Technol Educ Trop Appl Microbiol Microbial Biotechnol 1:567– 576 Zhao Y, Ji XL, Shen T et al (2020) Fungal endophytic communities of two wild Rosa varieties and the role of an endophytic Seimatosporium sp. in enhancing host plant powdery mildew resistance. Plant Soil 3:1–12

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Chapter 7

Tropical Endophytic Bacillus Species Enhance Plant Growth and Nutrient Uptake in Cereals Camila Cristina Vieira Velloso, Vitória Palhares Ribeiro, Chainheny Gomes de Carvalho, Christiane Abreu de Oliveira, Ubiraci Gomes de Paula Lana, Ivanildo Evódio Marriel, Sylvia Morais de Sousa, and Eliane Aparecida Gomes Abstract Several abiotic factors, such as nutrient deficiency and drought, contribute to reducing agricultural productivity in the world. Plant growth-promoting bacteria can enhance crop growth and sustainable crop production. Bacillus is the most common genus within the Firmicutes group and one of the most predominant plants endophytic bacteria. Once established within the plant, the ability of these endophytes to promote plant growth occurs due to several mechanisms that include the acquisition of essential mineral nutrients and modulation of phytohormones. Especially in tropical ecosystems, the ability of endophytic microorganisms to colonize the internal tissues of plants suggests an ecological advantage. The post-genomic era is allowing the characterization of unknown genes and the identification of genes expressed during colonization. A better understanding of how beneficial bacteria colonize different plant niches will lead to more successful and reliable use of bacterial inoculants. The commercialization of bioinoculants is a reality, however, the exploration of the more efficient use of these nutrients have the potential to increase the field of the inoculants and create confidence among the farmers for their use. Keywords Endophytic bacteria · Phytohormones · Abiotic and biotic stresses · Inoculant

C. C. V. Velloso · V. P. Ribeiro · I. E. Marriel · S. M. de Sousa Universidade Federal de São João Del-Rei (UFSJ), Praça Dom Helvécio 74, São João del-Rei-MG, MG 36301-160, Brazil C. G. de Carvalho · C. A. de Oliveira · U. G. de Paula Lana · I. E. Marriel · S. M. de Sousa Centro Universitário de Sete Lagoas (UNIFEMM), Av. Marechal Castelo Branco, Sete Lagoas, MG 35701-242, Brazil C. A. de Oliveira · U. G. de Paula Lana · I. E. Marriel · S. M. de Sousa · E. A. Gomes (B) Embrapa Milho e Sorgo, Rodovia MG 424—Km 45—Caixa Postal 285, Sete Lagoas, MG 35701-970, Brazil e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_7

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7.1 Introduction Cereals play an important role in the world’s agriculture economy, considering their area sown and annual production volume, being used as food, feed, and industry. Although maize, wheat, and rice are the most important to feed the world, other crops such as sorghum and millet are also relevant, especially in Asia and Africa (FAO 2019). The world’s population today is around 7 billion and is estimated to reach 9 billion by 2050. Challenges to feed the ever-growing population coupled with global climate change increase the need for sustainable and environmentally sound agricultural production (FAO 2019; Naumann et al. 2018; Ngumbi and Kloepper 2016). However, the productivity enhancement system is highly dependent on chemical inputs, especially nitrogen, phosphate, and potassium fertilizers (Ladha et al. 2016), which not only increases the production cost (Haygarth et al. 2014; Kvaki´c et al. 2018) but cause environmental adverse impacts such as groundwater pollution, soil degradation, micronutrient deficiency, eutrophication of water sources, toxicity to different beneficial organisms and plummeting of microbiota biodiversity, and overall management of ecology (Sharma and Singhvi 2017; Maheshwari and Annapurna 2017). Endophytic bacteria, microorganisms that spend at least part of their life cycle inside plants without causing apparent damage, have emerged as an economically and environmentally sustainable alternative to traditional methods. Microbial inoculants, characterized as products that contain strains of beneficial microorganisms to the plant growth and development, such as plant growth-promoting bacteria (PGPB) play an important role in the production of sustainable crops, reducing environmental impact and human health hazards. Various names have been given to PGPB according to their efficacy and use in plant ecosystem. Maheshwari (2010) has coined the term as plant growth- and health-promoting bacteria. Such organisms are capable to provide better adaptability and survival under biotic and abiotic stress conditions, and have the potential to mitigate the excessive use of pesticides and fertilizers in agriculture (Alori et al. 2017; Alori and Babalola 2018; Bashan et al. 2014; Singh et al. 2016). These are able to stimulate plant growth at different stages of development using direct mechanisms as phytohormones, enzyme production and nutrient uptake, and indirect mechanisms including biological control and induced systemic resistance (Nazir et al. 2018; Saini et al. 2015; Varma et al. 2017). Various workers consider the plant microbiome, i.e., the collective genomes of microorganisms living in association with plants, as a second genome, due to its close proximity between both partners and its impact on the host plant. It comprises a broad and diverse group of microorganisms, although most of them belong to relatively small phylogenetic group, comprising mainly of Firmicutes and Proteobacteria. The most important genera of Proteobacteria are Rhizobium, Agrobacterium, and Sphingomonas (α-proteobacteria); Burkholderia (β-proteobacteria); Enterobacter, Klebsiella, Pantoea, and Pseudomonas (γ-proteobacteria). Among all, Bacillus is the most common genus within the Firmicutes group followed by Paenibacillus and Staphylococcus (Wallace and May 2018; Rodriquez et al. 2019).

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Members of the Bacillus are reported as one of the most predominant plant endophytic bacteria presenting several plant growth-promoting traits. Once established within the plant, the ability of these endophytes to promote plant growth occurs because of mechanisms that include the acquisition of essential nutrients (biofertilization), such as nitrogen (N), phosphorus (P), and potassium (K) (Fig. 7.1), the modulation of the level of phytohormones, essential for plant development (Calvo et al. 2010), such as auxins, cytokinins, gibberellins, etc. (Bhattacharyya et al. 2015; Pérez-Flores et al. 2017). In addition, other mechanisms include synthesis and excretion of antibiotics and enzymes proteases, chitinases, bacteriocins, production of siderophores, biofilms, secretion of exopolysaccharide, volatile organic compounds, and induction of systemic resistance (Barriuso et al. 2008; Santoyo et al. 2016; Walker et al. 2011). Bacillus is promising candidate for use as plant microbial inoculants due to important traits to alleviate or eliminate the negative effects of saline, drought, and oxidative stresses. In addition, sporulation of this bacterial genus promotes its survival under different environmental conditions, thus facilitating the adaptation of strains to commercial formulation and field application (Ghyselinck et al. 2013; Pinter et al. 2017; Tiwari et al. 2019). Therefore, the association of cereals, such as maize, wheat,

Fig. 7.1 Plant nutrient uptake (NPK) enhancement mediated by plant growth-promoting bacteria (PGPB)

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rice, millet, and sorghum, with PGPB bacilli can increase productivity and food security, and reduce the use of agrochemicals and production costs contributing to a more sustainable agriculture. This chapter provides an overview of the importance of endophytic Bacillus from tropical soils associated with different cereals with main emphasis on plant nutrition.

7.2 Plant Colonizing Endophytic Bacteria Plant growth-promoting bacteria (PGPB) colonize the rhizosphere, the foliar surface (epiphytic) or the interior of plant tissue (endophytic) providing plants with nutrients and protection against biotic and abiotic stresses (Ahmad et al. 2008; Boddey et al. 2003; Doty et al. 2016; Franche et al. 2009; Santoyo et al. 2016; Maheshwari and Annapurna 2017). Although, most of the research on PGPB focuses on rhizobacteria, knowledge of endophytic bacteria has grown extensively in recent years creating a relatively new niche and very promising approach to the development of sustainable agriculture (Miliute et al. 2015; Santoyo et al. 2016; Xia et al. 2015). Currently, endophytic microorganisms have been reported from nearly all host plants studied, including crops of agronomic importance, natural and extreme conditions environments, wild and perennial plants (Nair and Padmavathy 2014; Yuan et al. 2014; Zinniel et al. 2002). Endophytic bacteria live, at least a part of their life cycle inside plants, apparently without causing any damage to their hosts (Assumpção et al. 2009), which differentiates them from phytopathogenic microorganisms. Even though roots have the highest number of endophytes compared to the shoot (Rosenblueth and Martínez-Romero 2006), endophytes have been isolated from flowers, fruits, leaves, stems, and seeds of various plant species (Kobayashi and Palumbo 2000; Melnick et al. 2008; Piccolo et al. 2010; Thomas et al. 2007). They present different mechanisms of colonization, particularly roots hence considered as a subgroup of rhizospheric bacteria that have acquired the ability to colonize plants without inducing the host defense pathway (Marquez-Santacruz et al. 2010; Misko and Germida 2002). Once within the plant, endophytic bacteria can exert a direct and more effective beneficial effect compared to rhizospheric bacteria due to consistent nutrient supply and, as they occupy the same habitat as phytopathogenic microorganisms, therefore efficient in disease control (Compant et al. 2010). In addition, being more competitive than non-endophytic microorganisms inside the host plant assist in the endophyte-plant interaction an evolutionary process controlled by genes of both organisms (Rosenblueth and Martínez-Romero 2006). According to life strategies, endophytes are classified as obligate or facultative organisms in nature. The obligate ones are those strictly dependent on the host plant for their growth and survival, usually transmitted by seeds and spread in the plant by vertical colonization or by the action of a vector. Facultative endophytes have some phases of the life cycle inside the host plant and another in which they live outside (Hardoim et al. 2008). They constitute the majority of endophytic microorganisms showing as characteristic of the biphasic lifestyle alternating between plant and

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Fig. 7.2 Endophytic bacteria colonization. Bacteria can colonize plants entering roots cracks and wounds, or hydrolyzing root cells. Other pathways include stomata, particularly in young leaves and stems, lenticels, and germinating seeds

rhizospheric soil. The distinction between the rhizosphere population and endosymbionts of a host plant may represent a true continuum, with microbes able to move between the soil, the rhizosphere, and inside the root (Farrar et al. 2014) (Fig. 7.2). Indeed, several species of microorganisms use the nutrient niche in the rhizosphere and change from a free-living condition to an endophytic state (Rosenblueth and Martínez-Romero 2006). Bacterial endophytes that were injected into stems moved to the roots and the rhizosphere, thereby confirming the existence of a continuous shift in microbial community within the root microbiome (Gaiero et al. 2013). A battery of different mechanisms that involve complex communication between partners and include motility, adhesion, plant-cell wall degradation, and escape from plant defences determines endophytic colonization. The highly competitive process, involve only those bacteria that can occupy spaces or niche near the root and get nutrients may succeed. The most common mode of entry of these bacteria into plant tissues is through cracks in the primary and lateral roots (Agarwal and Shende 1987; Liu et al. 2006; Sørensen and Sessitsch 2006; Sprent and de Faria 1998) (Fig. 7.2). Root cracks allow plant metabolites to exudate, becoming sites that attract these bacteria (Hallmann et al. 1997). Although, endophytic bacteria usually enter the host plant from the roots, shoot, including stomata, particularly young leaves and stems (Roos and Hattingh 1983), lenticels, which are usually present in the stem and root periderm (Scott et al. 1996), flowers and cotyledons (Zinniel et al. 2002). Once inside the plant, endophytic bacteria can systematically infect adjacent plant tissues via xylem or phloem vessels.

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On the other hand, plants can select endophytic bacteria through steps that function as filters primarily in the rhizosphere, then rhizoplane, and endosphere. The rhizosphere is described as the main compartment or “gateway” that deeply influences the plant’s endophytic microbiome. The different physicochemical and biological properties of the carbon-rich molecules and antimicrobial compounds exuded in this region may favor the growth and multiplication of certain groups of microorganisms while inhibit others. Rhizoplane functions as a second selection point for microorganisms, where only those capable of binding to the root surface are allowed to enter the endosphere (Edwards et al. 2015; Reinhold-Hurek et al. 2015). On the other hand, the plant’s immune system actively excludes specific groups of microorganisms (Lundberg et al. 2012). Root colonization often begins with chemotaxis, i.e., bacterial recognition of certain compounds in root exudates. Although there is no direct evidence of the presence of a specific compound, flavonoids are considered as an important player in plant-microorganism communication (Shaw et al. 2006). Once in the rhizosphere, endophytic bacteria must bind to the root surface (rhizoplane) to reach entry sites such as lateral emergence and root tips or regions with cracks caused by pathogens or predators. Bacterial traits such as motility, polysaccharide production, and adhesins are important in the root surface adhesion process (Hori and Matsumoto 2010). As they bind to the root surface, bacteria multiply resulting in the establishment of microcolonies or biofilms thus, become successful in the colonization process. The host penetration process can be passive or active. In passive, the bacterium uses fissures already present in the root and in the active, penetration occurs through the production of lipopolysaccharides, flagella, pili, and quorum sensing (Böhm et al. 2007; SuárezMoreno et al. 2010). In the active process, secretion of cell wall degrading enzymes such as pectinases and cellulases are described as important mechanisms for the penetration and colonization of bacteria within host plants (Compant et al. 2005). As endophytic bacteria enter the plant, they respond to host stimuli to induce the cellular processes necessary for the maintenance of the endophytic stage and distribution to cortical tissue of the root. At this point, they can multiply within the tissues often reaching high populations, depending on the stage of plant development (Hardoim et al. 2008). Migration of root bacteria to shoot tissues requires the production of cell wall degrading enzymes. It can also occur through xylem elements, directed by plant transpiration, which allow the movement of bacteria mainly reaching the leaf tissues. Only few bacteria can migrate and adapt to the shoot, as this colonization requires specific physiological signals to occupy plant niche (Hallmann 2001). In general, endophytic microbial communities are less diverse than the rhizospheric communities, for both bacteria and fungi. This suggests that roots select the endosphere community members that consequently present more defined groups (Bulgarelli et al. 2013). The bacterial endophyte community patterns in leaf, stem, and root of three tropical rainforest plant species show a lower diversity of OTU richness, species richness, and community diversity (inversed Simpson’s index) in comparison to that of rhizospheric soil community (Haruna et al. 2017). This emphasizes that, the bacteria rhizospheric community from these three plant species is relatively

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distinct from the endophytic community. Recent studies from our research group show that maize root-associated microbial communities have lower diversity indices than the rhizospheric communities (Gomes et al. 2018). These results are evidenced and consistent with previous studies showing that maize endophytic microbiota differ from those of the rhizosphere (Edwards et al. 2015; Miliute et al. 2015; Robbins et al. 2018).

7.3 Endophytic Bacillus and Plant Growth Promotion in Tropical Soils Tropics occupy approximately one-third of the Earth’s surface, with different climate, vegetation, geomorphology, lithology, and, consequently, soils in the region which are more diverse than temperate and arctic soils (Kalpage 1974), which contributes to the microorganism diversity. There is a growing interest in understanding the role of endophytic microorganisms in tropical soils. The investigation of bacterial diversity in these soils may help to describe new species and to elucidate traits related to plant growth promotion under adverse tropical conditions. Major factors that constrain tropical soil fertility and sustainable agriculture are low nutrient capital, moisture stress, erosion, high P fixation, and high acidity with aluminum toxicity (Santos et al. 2010; Camenzind et al. 2017; Garland et al. 2018). Phosphate soluble fertilizers applied to soils can be complexed by adsorption to iron and aluminum oxides (mainly in clayey tropical soils) and calcium precipitation (alkaline soils), making it unavailable to plants (Novais and Smyth 1999). Phosphorus can also be complexed in organic form reaching values of up to 80% of total P in no-till soils (Marschner et al. 2006). The fragility of many tropical soils limits food production in annual cropping systems. Since some tropical soils under natural conditions have high biological activity, an increased use of the biological potential of these soils to counter the challenges of food production problems is proposed (Cardoso and Kuyper 2006). Phosphate solubilizing and mineralizing microorganism have a high potential to be used in the management of P deficient soils. The mechanisms of P solubilization by PGPB are associated with the production of organic and inorganic acids, proton excretion, and phosphatase activity. Organic acids decrease the rhizosphere pH favoring the solubility of precipitated P forms. They can compete or even replace phosphate sorbed on the surfaces of soil clays and chelate Al and Fe avoiding thus the precipitation of phosphate (Vega 2007). Among the common members of PGPB community, Bacillus is the most naturally abundant and universally present endophytic genus in tropical plants (Tiwari et al. 2019). Although Bacillus is well known, there is still a range of information on endophytes that needs to be interpreted in tropical soils so that new metabolites and biotechnological characteristics of these bacteria can be used in medicine, industry, and agriculture.

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Bacillus comprises a heterogeneous group of Gram-positive bacteria widely distributed in the environment, consisting of approximately 360 species that have distinct physiological, metabolic, and phenotypic characteristics (www.bacterio.net/ bacillus.html). Numerous Bacillus sp. are known to enhance nutrient solubilization and facilitate nutrient mobilization in the soil. Our research group reported that maize plants inoculated separately with different Bacillus strains capable of producing indole-3-acetic acid (IAA) and solubilizing phosphate enhanced root system, dry matter, and nutrient accumulation in hydroponics. Under field conditions, strains increased maize yield and P grain accumulation by around 36 and 58%, and P grain in 21% in soils with no P added. Even in soils fertilized with triple superphosphate, maize yield increase and P grain accumulation was observed around 20% after inoculation comparing to non-inoculated control (unpublished results). In another study, pearl millet (Pennisetum glaucum) seeds inoculated with endophytic Bacillus strains isolated from maize grown in the Brazilian Cerrado, showed increased shoot and root dry weight, N and P content in the roots and N, P, and K in the shoot, promoting growth and nutrient uptake in greenhouse conditions. Probably the main mechanism involved in these processes are the production of IAA, siderophores, and solubilization of phosphate (Ribeiro et al. 2018). Interestingly, these strains showed high organic acid production, which is one of the mechanisms involved in solubilization of mineral phosphates, due to lowering soil pH (Abreu et al. 2017). Other examples of endophytic Bacillus in tropical soil show that inoculation of strains isolated from medicinal plants, crops and weed enhanced seed germination, and seedlings vigor of pearl millet crop plants. In addition, the vegetative (height of the plant, number of basal tillers, fresh and dry weight) and reproductive growth parameters (early flowering, length and girth of ear heads, 1000-seed weight, plant height, and tillering) were higher than control due to the treatment of maize seeds with the endophytic bacteria (Chandrashekhara et al. 2007). The Bacillus strains were also efficient in reducing the incidence of downy mildew caused by Sclerospora graminicola under greenhouse and field condition, demonstrating their potential as a biocontrol agent (Chandrashekhara et al. 2007). In addition to agricultural crops, various studies have shown evidence of the benefits of Bacillus endophytic in forestry of Eucalyptus, particularly in tropical and subtropical regions, due to its rapid growth, adaptability, and the commercial value of its wood (Brooker 2000). However, the Eucalyptus–endophytic bacteria interaction is poorly described, and the majority of previous studies have focused on rhizosphere microorganisms (Bonito et al. 2014; Silva et al. 2014). One of the first studies describing Bacillus, including B. licheniformis and B. subtilis, as endophytes of eucalyptus exhibited an increase of the root and shoot growth of plantlets after inoculation under greenhouse conditions, during the summer and winter seasons (Paz et al. 2012). Other studies have shown evidence of the benefits of endophytic inoculation in eucalyptus plantlets; for instance, increasing the rooting indexes and vegetative biomass or acting as biocontrol agents in improving plant resistance when challenged with different pathogens (Ferreira et al. 2008; Mafia et al. 2005; Procópio et al. 2009). Related to nutrient efficiency, the potential for biological nitrogen fixation

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(BNF) of endophytic species was assessed in E. urograndis roots using culturedependent and culture-independent techniques. The data suggests that Eucalyptus benefit from BNF, with many abundant genera closely related to nitrogen-fixing bacteria. Under N-depleted media, 25% of the bacterial isolates are able to grow and present the nif H gene. As the most dominant members were related to Bacillus, the conclusion is that the naturally high abundance of these bacteria makes them the most promising bacterial inoculant for plant growth promotion. In addition to high P fixation and aluminum toxicity, tropical agriculture suffers the effect of the continuous attack of plant pathogens as these environments present ideal water, temperature, and nutrient conditions for their proliferation. The identification and development of locally adapted biological control agents are extremely pertinent as native strains have greater adaptability, performance, and suitability than introduced microorganisms. Considering the seriousness of diseases in tropical agriculture, native B. amyloliquefaciens, B. cereus, B. megaterium, and B. pumilus strains from tropical soils of Trinidad were isolated and characterized as antibiotic lipopeptide producers, such as iturin, bacillomycin, bacilysin, fengycin, surfactin, and zwittermycin. Testing of these Bacillus species against pathogens such as Alternaria, Fusarium, Ralstonia, Cercospora, and Colletotrichum revealed greater antagonistic activity of all lipopeptide produced by B. amyloliquefaciens strains as compared with non-producers being promising for the development of bioagents suitable for disease management in tropical conditions (Saravanakumar et al. 2018). Antifungal lipopeptides inhibiting plant pathogens as F. moniliforme as well as inducing the up-regulation of pathogenesis-related (PR) genes of host plants (systemic acquired resistance) were also reported in endophytic Bacillus spp. isolated from maize from Indian popcorn and yellow dent corn. The presence of antifungal iturin A, fengycin, and bacillomycin were also detected using MALDI-TOF mass spectrometry (Gond et al. 2015). In tropical ecosystems, the ability of endophytic microorganisms to colonize the internal tissues of plants suggests an ecological advantage. Mangrove forests, typical tropical ecosystems situated between land and sea, are among the most productive and diverse communities worldwide, particularly in Brazil, Indonesia, and Australia. These ecosystems are important sources of endophytic microorganisms with biotechnological potential, which deserves further studies (Sebastianes et al. 2017). Interesting, Bacillus is the most frequent genus, comprising 42 and 28% of the endophytic isolates from plant species from two mangrove systems in Brazil. In other study, Bacillus spp. isolated from mangrove trees in Malaysia show efficacy in promoting seedling growth in rice. The inoculation of rice seeds with endophytic strains of B. cereus and B. amyloliquefaciens significantly increased the root and shoot length, suggesting that endophytic bacteria from mangrove trees can increase the fitness of rice seedlings under controlled conditions (Deivanai et al. 2014). Other studies evaluated the enzyme production of endophytic Bacillus from mangrove forest in India and Brazil. Enzymes protease and endoglucanase activity are observed in 70% of the isolates and bacteria exhibit the highest activity rates for amylase, esterase, and endoglucanase. In addition, the antimicrobial activity against important pathogens,

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such as Fusarium, Staphylococcus aureus, Vibrio parahaemolyticus, and V. anguillarum, indicating biological control potential have also been observed (Castro et al. 2014).

7.4 Bacillus in Post-Genomic Era The development of bioinformatics tool coupled to constant innovation in sequencing platforms enabled genome sequencing and annotation, metabolic pathway construction, new bioactive molecules as well as their biochemical properties allowing the clarification of new mechanisms related to plant growth-promoting (Blin et al. 2017; Blom et al. 2016; Conesa et al. 2005; Kanehisa et al. 2016; Koskinen et al. 2015; Seemann 2014). In addition, advances in DNA sequencing technologies reduced the sequence cost per base, allowing sequencing complete genomes with an affordable price, allowing a deeper and global knowledge that considers gene and metabolic pathways instead of isolated information. Complete or draft of PGPB genome allows the characterization of gene content, genome structure, PGP mechanisms, and in silico physiological, ecological, and evolution studies (Belbahri et al. 2017; Chaudhry et al. 2017; Ma et al. 2018). The first Gram-positive PGPB to have the fully sequenced genome mapped was B. amyloliquefaciens subsp. plantarum, FZB42T (Chen et al. 2007). Subsequently, several genomes of Bacillus capable of PGP and acting on biocontrol were available (Table 7.1). To date, more than 4,600 genomes of this genus have been sequenced, ranging from approximately 0.56 to 9.84 Mb in different assembly level and are available in the GenBank database (https://www.ncbi.nlm.nih.gov/genome/browse/#!/pro karyotes/bacillus). The genome content of different endophytic Bacillus strains reveals that a significant portion of the genome encodes proteins related to molecules with biotechnological applications. A comparative study of 31 Bacillus genomes showed that plantrelated Bacillus strains contain more genes involved in intermediary metabolism and secondary metabolites production than non-plant associated strains. In addition, plant-related Bacillus strains possess additional genes involved in utilization of plant-derived substrates and synthesis of antibiotics, which have arisen via horizontal gene transfer events during the evolutionary process (Zhang et al. 2016). For example, endophytic B. velezensis CC09 genome, capable of promoting growth and preventing fungal disease in plants, is related to nonribosomal peptide synthetase, polyketide synthetase, as well as genes related to iron acquisition, colonization, and synthesis of volatile organic compounds (Cai et al. 2016). Clusters of genes responsible for antifungal (fengicin, surfactin, bacillisin) and antibacterial metabolites (butyrosine, bacillene, difficidine, macrolactin, surfactin, bacillisin), as well as genes associated with PGP including phosphate solubilization, siderophores production, and pathogen growth inhibition were also found in the genome of the endophytic B. velezensis LDO2 (Chen et al. 2019).

Nonribosomal peptide synthetase for the production of antibiotics such as surfactin, bacillibactin, and bacilysin, indole3-acetaldehyde and 2,3-butanediol, swarming and biofilm formation Sporulation transcription factors related to biofilm formation, Sun et al. (2015) antimicrobial biosynthesis, bacteriocins, siderophore-synthesis, and production of endoglucanases, cellulases, and glucanases Synthesis of polyketide and nonribosomal peptides such as Cai et al. (2016) surfactin, iturin A, fengycin, bacillibacti, genes associated with iron acquisition, colonization, and volatile organic compounds synthesis Phosphate utilization, iron acquisition, biosynthesis of exopolysaccharides and bacteriocin production Nitrogen fixation, siderophore, cobalamin, spermidine, phenazine, and acetoin synthesis

B. pumilus INR7

B. amyloliquefaciens XK-4-1

B. velezensis CC09

B. mycoides M2E15

B. flexus KLBMP 4941

Wang et al. (2017)

Yi et al. (2016)

Jeong et al. (2014)

Gold et al. (2014)

Operons for biosynthesis of antifungal compounds, a bacillibactin-like siderophore, antibiotic bacilysin, and biosynthesis of volatile compounds

B. mojavensis RRC101

Reference

Plant growth promotion genes, operons, and coding DNA sequence (CDS)

Bacillus strain

Table 7.1 Examples of Bacillus strains with complete genome sequence and plant growth promotion properties

(continued)

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Nitrogen metabolism pathway and two main transcriptional factor genes, glnR and tnrA responsible for the regulation of nitrogen fixation Heat shock resistance, hydrocarbon metabolism, heavy metal tolerance, biofilm formation, siderophore, and IAA biosynthesis Indole-3-acetic acid acetyltransferase, indole-3-acetaldehyde dehydrogenase; gene clusters including ribosomally synthesized peptides, nonribosomal peptide synthetases, and polyketide synthases

Proteins involved in the biosynthesis of IAA, synthesis of Pinto et al. (2018) volatile compounds, nitrate reduction pathways, protein nifU, and a cysteine desulfurase nifS, which are involved in the Fe-S cluster assembly and required for the activation of nitrogenase, nitric oxide synthase, phytase, and siderophores synthesis, ABC transporters for iron and iron uptake

B. paralicheniformis KMS 80

B. pumilus SCAL1

B. velezensis PEBA20

B. amyloliquefaciens subsp. plantarum Fito_F321

Kong et al. (2018)

Mukhtar et al. (2018)

Annapurna et al. (2018)

ACC deaminase, several putative siderophore biosynthesis, Yaish (2017) binding, and transport proteins, ampicillin-resistant beta-lactamase proteins, and biosynthesis gene of locillomycin, asukamycin, and iturin antibiotic

B. aryabhattai SQU-R12

Reference

Plant growth promotion genes, operons, and coding DNA sequence (CDS)

Bacillus strain

Table 7.1 (continued)

(continued)

168 C. C. V. Velloso et al.

Secondary metabolite production, including 3 nonribosomal Wemheuer et al. (2018) polyketide synthetase, bacteriocin production, paeninodin, and siderophores biosynthesis Virulence, disease and defense, stress response, iron, phosphorous, and sulphur metabolism Siderophore production, nutrition utilization such as nitrogen, magnesium, phosphate, and potassium, growth-promoting hormones (IAA) and stress response

B. mycoides GM6LP

B. toyonensis COPE52

Bacillus sp. MHSD28

Makuwa and Serepa-Dlamini (2019)

Contreras–Pérez et al. 2019

Potshangbam et al. (2018)

Antioxidant enzymes, such as catalase, peroxidase, and superoxide dismutase, pathways related to phosphorous solubilization, iron uptake, cellulose degradation, chitinolytic activity, glucanase, acetoin dehydrogenase, protease, trehalose metabolism, exopolysaccharides, cytokinin, and tryptophan biosynthesis, as well as nitrogen-fixing proteins

B altitudinis Lc5

Reference

Plant growth promotion genes, operons, and coding DNA sequence (CDS)

Bacillus strain

Table 7.1 (continued)

7 Tropical Endophytic Bacillus Species … 169

170

C. C. V. Velloso et al.

B. paralicheniformis strain KMS 80, isolated from rice root is able to fix nitrogen presenting almost 21 genes involved in nitrogen metabolism pathway such as glnA, glnL, glnR, glnT, tnrA, and nif H gene, etc. (Annapurna et al. 2018). In the genome of Bacillus sp. MHSD28 strain, endophytic bacteria isolated from the medicinal plant Dicoma anomala, several genes associated with PGP have also been identified (Makuwa and Serepa-Dlamini 2019). In addition, due to the growing number of sequenced endophytic Bacillus genomes, the identification of bioactive compounds has been predicted and their production confirmed, revealing that endophytic bacillus species are underexploited sources of new molecules of biotechnological interest (Radhakrishnan et al. 2017; Lopes et al. 2018). For example, genome studies of B. amyloliquefaciens showed an increase of new strain-specific secondary metabolite clusters that play key roles in pathogen suppression and PGP (Belbahri et al. 2017). Recently, our research group sequenced the genome of two PGP strains: B. thuringiensis B116 and B. megaterium B119 isolated from tropical maize capable of increasing yield and phosphorus content in maize grains in field experiments (Vieira Velloso et al. 2020). The draft genome of these two strains shows the genes related to endospore formation, chemotaxis, motility, competition in the rhizosphere, and several mechanisms of PGP. Both Bacillus species are able to produce exopolysaccharides (EPS) and fix nitrogen. However, B. megaterium produces higher amounts of IAA and siderophores, whereas B. thuringiensis is characterized as the best biofilm producer and is capable to solubilize more insoluble phosphate (Vieira Velloso et al. 2020). Overall, new molecular and genomic techniques accelerate the identification of bioactive compounds useful for agricultural and medical applications; reveal mechanism and pathways; and help to optimize in vitro isolation and biochemical characterization. Moreover, these techniques allow rapid identification of microorganisms and enable the characterization of microbiome diversity, since uncultivable microorganisms can also be detected. Thus, understanding the dynamics of the microbial community in different environments increases the discovery of new proteins and metabolites and the comprehension of stress tolerance and biotechnological applications (Hirel and Lea 2018; Imam et al. 2016; Krishnamurthy et al. 2018; Upadhyay et al. 2017).

7.5 Commercialization and Challenge of Bacillus Biotechnological Products Bacillus is one of the main microorganisms involved in the generation of biotechnological products for agriculture, representing the most important group for use in biological control in the form of insecticides, fungicides, bactericides, nematicides, as well as stress tolerance stimulants, and plant growth promoters. Among bacterial biocontrol agents, Bacillus species account for over 50% of marketed products, with B. thuringiensis contributing over 70% of this market (Ongena and Jacques

7 Tropical Endophytic Bacillus Species …

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2008). This is due to different properties of this group of bacteria, including the ability to form endospores, allowing them to adapt to extreme abiotic conditions such as temperatures, pH, radiation, desiccation, ultraviolet light, or pesticide exposure (Bahadir et al. 2018). In addition, endospores enable greater resistance of stock products by increasing shelf life of Bacillus-based products. The commercial success of a PGPB-based product requires viable and economical market demand, consistent and broad spectrum of action, safety and stability, low cost and availability of adjuvants, marketing of bioinoculant products, and interaction between academia and industry. As part of the future of bioinoculants, research should focus on optimizing growth conditions and increasing the shelf life of PGPBbased, the product should not be toxic to plants and animals must tolerate severe environmental conditions, increase crops production and be cost-effective for farmers use (Mustafa et al. 2019). Most of these conditions are observed in Bacillus-based products, which have great potential to be used in integrated agricultural production systems, which justifies the screening and characterization of new strains. Many products both soild and liquid of PGPB formulated with Bacillus strains are already available in the market in different countries where they are applied as biofertilizers, phytostimulators, rhizoremediators, and bio-pesticides to attain varied benefits for better plant growth (Table 7.2). Recently, the microbiology research group of Embrapa Maize & Sorghum in a partnership with the Bioma Company (bioma.ind.br) registered and started the commercialization of BiomaPhos® , a consortium of two Bacillus strains, B. megaterium (CNPMS B119) and B. subtilis (CNPMS B2084) inoculants for phosphate solubilization. This liquid inoculant, recommended for seed treatment or in sowing furrow spray, associates with the plant since the beginning of root formation. The bacteria present in the product multiply and colonize the plant rhizosphere initiating the production of organic acids that solubilize the phosphorus fixed calcium, aluminum, and iron present in the soil portion in contact with the plant roots (rhizosphere), making it readily available for plant absorption and assimilation. In addition, BiomaPhos® also acts in the mineralization of phosphorus present in soil organic matter (phytate), giving greater contribution to the crop. The Biomaphos® is an interesting example of the different stages between the beginning of the scientific research and the product available to the farmers in tropical conditions. One of the strains, B. megaterium (CNPMS B119) was isolated from rhizosphere of tropical P-efficient maize genotypes and characterized as P solubilizing and mineralizing, presenting high phosphatase activity (Oliveira et al. 2009). The other strain, B. subtilis (CNPMS B2084), is an endophytic strain isolated from maize roots, characterized as high organic acids producer and P solubilizer (Abreu et al. 2017). Both strains separately can increase biomass, shoot nutrient content, and root surface area in controlled and field condition. When maize was inoculated with strain B2084, there was 12% increase in yield and the inoculation with B119 improved grain P accumulation by 21% comparing with the non-inoculated control. Under TSP fertilization, there was a significant increment on yield of approximately 26% of maize plants inoculated with B119. Moreover, plants inoculated with B119 strain showed 24% increase in P grain content comparing with the non-inoculated

Company

Total Biotecnologia/Biotrop

Bioma/Simbiose

Special Biochem (P) Ltd

Total Biotecnologia/Biotrop

FMC Corporation

Varsha Bioscience And Technology India Private Ltd

Biosoja

Total Biotecnologia/Biotrop

Bayer

Total Biotecnologia/Biotrop

Product name

Accelerate max

BiomaPhos

Bio-Phospho

Enduro

Nemix C

Phosphomax

Rizolyptus

Rudder

Serenade Prime

Vult

Brazil

Australia

Brazil

Brazil

India

Brazil

Brazil

India

Brazil

Brazil

Country

Phytohormones, antibiotics, hydrolytic enzymes, elicitation of plant defense

Higher yields, better crop uniformity, improved harvest crop quality, improved shelf life

Production of exopolysaccharides, biofilm

Phytohormones, nitrogen fixation

Phosphate solubilization

Phytohormones, nutrients uptake, biofilm

Nutrients uptake, nitrogen fixation, biological control

Phosphate solubilization

Phosphate solubilization/mineralization

Nutrient solubilization, mineralization of organic compounds, acid organic production

Benefit/mechanism

B. subtilis

B. amyloliquefaciens

B. amyloliquefaciens

B. subtilis

B. megaterium

B. subtilis B. licheniformis

B. pumilus

B. subtilis

B. megaterium, B. subtilis

B. subtilis, B. amyloliquefaciens, B. pumilus

Composition

Crops

Vegetable crops, berries, tree crops

Crops

Eucalyptus

Crops

Sugarcane

Crops

Crops

Crops

Crops

Suitable for

Table 7.2 Outline of selected PGPB-based Bacillus formulation available commercially in the market of tropical countries

http://biotrop.com.br/

https://www.crop.bayer.com.au/findcrop-solutions/by-product/bayer-biolog ics/serenade-prime#tab-2

http://biotrop.com.br/

http://biosoja.com.br/media/89_RIZ OLYPTUS.pdf

https://www.indiamart.com/proddetail/ phosphobacteria-bio-fertilizer-115502 43355.html

https://www.fmcagricola.com.br/con teudo/produtos/boletim_tecnico_nemix_ a4.pdf

http://biotrop.com.br/

https://www.indiamart.com/proddetail/ bio-phospho-bio-fertilizer-7618252062. html

https://www.bioma.ind.br/product/ bioma-phos

http://biotrop.com.br/

Site

172 C. C. V. Velloso et al.

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control (de Sousa et al. 2020). After testing for different mechanisms of PGP in vitro, the strains were co-inoculated in maize seeds, tested in controlled conditions and in the field. The selection of the adjuvant and method required for inoculation is based on the microorganism’s viability, crops, and application method. Positive results in the field attract the attention of inoculant-producing industries, an important step for the formulation, large-scale production, product marketing, and training to farmers.

7.6 Conclusion and Future Prospects Tropical endophyte Bacillus is well known for their capacity to confer plant growth promotion and to increase resistance toward various diseases as well as abiotic stresses. However, some strains fail to confer these beneficial effects when applied in the field. The lack of various characteristics, which are important for efficient colonization of the plant environment and the limited supply of the appropriate formulation, could explain poor plant host colonization. Further analysis of sequenced genomes, the characterization of unknown genes and the identification of genes expressed during colonization may lead to a better understanding on how beneficial bacteria colonize different plant niches, thus result not only in scientific knowledge on plant microbe interactions, but also in a more successful and reliable use of bacterial inoculants. The use of PGPB for mineral solubilization and N fixation has progressed well, but yet to be done more for zinc and potassium solubilization and sulphur oxidation. The exploration of the more efficient use of these nutrients has the potential to increase the field of the inoculants and create confidence among the farmers for their use. In order to accomplish this, there is a need to invest more in research regarding plant–microorganism–soil interaction, growth condition optimization, tolerance to adverse environmental condition, and provide higher yield and longer shelf life with cost-effective for farmers for long-term applications.

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Chapter 8

Biotechnology and Bioinformatics of Endophytes in Biocontrol, Bioremediation, and Plant Growth Promotion Houda Ben Slama, Hafsa Cherif-Silini, Ali Chenari Bouket, Allaoua Silini, Faizah N. Alenezi, Lenka Luptakova, Armelle Vallat, and Lassaad Belbahri Abstract Endophytes have been known for more than a century and recent studies highlighted their endless potentialities in plant growth promotion through several direct and indirect mechanisms. Competent microbial endophytes have been acknowledged in several fields including medicine, industry, pharmacology, bioremediation, and phytoremediation of pollutants due to their safe handling and environment-friendly effects. Modern genomic approaches are considered an effective tool to get a better knowledge of the microbial modes of action. This chapter focuses on endophytes taxonomic affinities and lifestyle, their plant growthpromoting mechanisms, their applications as well as the potential of emerging “omic” tools including genomic, transcriptomic, metabolomics, and proteomics to shed the light on the wealth of their genomic and metabolic potentialities. H. B. Slama · L. Belbahri (B) NextBiotech, 98 Rue Ali Belhouane, 3030, Agareb, Tunisia e-mail: [email protected] H. Cherif-Silini · A. Silini Laboratory of Applied Microbiology, Department of Microbiology, Faculty of Natural and Life Sciences, University Ferhat Abbas Setif-1, Setif, Algeria A. C. Bouket Plant Protection Research Department, East Azarbaijan Agricultural and Natural Resources Research and Education Center, AREEO, Tabriz, Iran F. N. Alenezi Environmental Technology and Management Department, College of Life Sciences, Kuwait University, Kuwait City, Kuwait L. Luptakova Department of Biology and Genetics, Institute of Biology, Zoology and Radiobiology, University of Veterinary Medicine and Pharmacy, Kosice, Slovakia A. Vallat Neuchatel Platform of Analytical Chemistry, Institute of Chemistry, University of Neuchatel, Neuchatel, Switzerland L. Belbahri Laboratory of Soil Biology, University of Neuchatel, Neuchatel, Switzerland © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_8

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Keywords Rhizosphere · Genomics · Omics · Endophytes · Bioremediation

8.1 Introduction Since last decade, microbial endophytes have attracted attention. They are occupying a considerable position due to their ubiquitous association with almost all plants (Nair and Padmavathy 2014; Hardoim et al. 2015; Selim et al. 2017; Sharma et al. 2018; Goulart et al. 2019). Therefore, extensive studies have provided information about their endless potentialities in promotion of plant growth (Jasim et al. 2014; Cheffi et al. 2019; Slama et al. 2019) and inhibition of phytopathogens (Mefteh et al. 2017; Slama et al. 2018; Cherif-Silini et al. 2019). In addition to that, endophytes have been exploited in several other fields such as medicine, industry, pharmacology, bioremediation, and phytoremediation of pollutants (Eevers et al. 2015; Wani et al. 2015; Ma et al. 2016; Kumar and Verma 2018; Paramanantham et al. 2019). Modern next-generation sequencing involving genomic, proteomic, metabolomics, and metatranscriptomic technologies, have given deep learning of endophytic potentialities as well as mechanisms and metabolic pathways of secondary metabolites (Fakruddin and Mannan 2013; Finkel et al. 2019; Hong et al. 2019; Srivastava et al. 2019). Based on account of informations, this paper first attempts to define endophytes, followed by a brief insight into bacterial and fungal classification and taxonomic diversity. This chapter is also an account on role of endophytes in plant growth-promoting activities via direct and indirect ways. Their widespread environment-friendly applications in biotic and abiotic stress alleviation, in medicinal, industrial, and environmental applications have also been described. An overall overview of the advanced “omic” tools that could be used to get complete informations about endophytic genome and proteome functions and their interactions with hosts, potentialities, and secondary metabolites.

8.2 Definition of Endophytes Microbial endophytes have been known for more than a century, they mainly include fungi, bacteria, and actinomycetes. Their definition changed over time, in 1866 the term “endophyte” was first introduced by de Bary, it was originated from the Greek words endon: within and phyte: plant (Bary 1866). In 1926 endophytic behavior was defined as a particular stage (symbiotic mutualism) in the bacterial life cycle (Perotti 1926). From that moment, endophytes were defined as microorganisms being isolated from host plants after surface sterilization (Henning and Villforth 1940). Hollis defined endophytes more accurately as being microorganisms existing inside plant organs without causing disease symptoms (Hollis 1951). Several other definitions, differing from one another, were attributed to the term endophyte. Quispel

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(1992) mentioned that they are microorganisms that establish beneficial cooperation (endosymbiosis) with plants. In the same year, Kado (1992) included neutral bacteria (reside in the interior of living plants and benefit from a secure residence) to the endophytic community. In 1997, James and colleagues stated that all microorganisms colonizing internal plant tissues, including active and latent pathogens were considered endophytes (James et al. 1997). In agronomy, endophyte definition was expanded to cover all microorganisms emerging from surface-sterilized plant tissues and establishing mutualistic associations with host plants, but cause no symptoms of the disease (Hallmann et al. 1997; Azevedo et al. 2000). Schulz and Boyle (2006) defined endophytes as microorganisms colonizing internal plant tissues without causing any injuries and or adverse reaction on their host, whereas Thrall et al. (2007) pointed out that endophytes result from a positive selection to invade the plants’ tissues, during at least a period of their life cycle and perform mutualistic associations with them. The concept of endophytism was defined in several ways, however many scientists approved that endophytic microbial communities reside inside plant tissues with no harmful effect to hosts (Johnston-Monje and Raizada 2011; Hardoim et al. 2012; Gupta et al. 2013; Sarethy et al. 2019).

8.3 Endophytes Ongoing Researches and Major Trends An active international community has specialized in endophyte research (Fig. 8.1). Ongoing researches are multidisciplinary and involve many fields mainly Plant

Fig. 8.1 Bar-chart of international scientific community studies on endophytes

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sciences, Microbiology, Mycology, Biotechnology, Ecology, and Agronomy. The publication rate was doubled during last 5 years suggesting that the field is more and more attractive to researchers. USA, China, Germany, and India are the main countries for such scientific research.

8.4 Endophyte Taxonomic Affinities Endophyte taxonomic affinity is constantly updated by the huge mass of sequences that are being deposited in databases. In this report, we checked the taxonomic affinity of endophytes by monitoring bacterial 16S-rDNA and fungal ITS-rDNA sequences in GenBank. Two taxonomic divisions have been checked the phylum and the genus levels. a. Bacterial endophytes taxonomic affinities Our analysis documented that bacterial endophyte communities are dominated by proteobacteria (57.24%). This is in line with the results reported by Santoyo et al. (2016) and Belbahri et al. (2017). α, β, γ, and δ proteobacteria represented respectively 17.67, 22.94, 16.6, and 0.03% of the reported bacterial endophyte community in GenBank. Less abundant phyla were represented by Firmicutes (18.38%), Actinobacteria (13.89%), and Enterobacteria (8.74%). Remaining phyla represent all together lesser than 2% of the endophytic bacterial communities (Fig. 8.2). Similar results have also been reported in many endophytes targeted studies (Cheffi et al. 2019; Cherif-Silini et al. 2019; Slama et al. 2018, 2019). The most commonly reported endophytic genera are Burkholderia (16.88%), Bacillus (15.13%), Methylorubrum (12.04%), Enterobacter (6.02%), Herbaspirillum (5.94%), Streptomyces (5.43%), Pseudomonas (5.41%), and Pantoea (4.37%). (Alenezi et al. 2016; Slama et al. 2018, 2019). b. Fungal endophytes taxonomic affinities Our survey of fungal endophyte ITS-rDNA attested that belongs to Ascomycota (96.82%). Basidiomycetes represented 3.06% and Glomeromycota represented only 0.12%. These results corroborate earlier findings (Mefteh et al. 2017, 2018, 2019; White et al. 2019; Haro and Benito 2019). At the genus level Ustilago (13.42%), Fusarium (5.82%), Gibberella (5.7%), Colletotrichum (4.96%), Alternaria (4.48%), and Diaporthe (4.47%) dominated fungal endophyte communities (Fig. 8.3).

8.5 Endophyte Lifestyle The host-associated microbial communities are classified into obligate and facultative endophytes. Obligate endophytes are culture-independent and are revealed through molecular approaches, whereas facultative endophytes are culture-dependent and

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Fig. 8.2 Pie-chart of endophytic bacteria community based on 16S-rDNA

can be revealed through the application of diversified nutrient media (Christina et al. 2013; Goulart et al. 2019; Srivastava et al. 2019). These approaches have several advantages and drawbacks that are discussed in the two following sections. a. Culture dependent approach Cultivable endophytes could be easily isolated, manipulated, and further exploited in the development of different fields (agricultural, medical, industrial, etc.) as reviewed by Maela and Serepa-Dlamini (2019). The inherent limitation of this approach is that it is estimated to detect 0.1–1% of the existing microbiome (Stewart 2012; Belbahri et al. 2017; Mefteh et al. 2017, 2019).

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Fig. 8.3 Pie-chart of endophytic fungal community based on ITS-rDNA

b. Culture-independent approach The main advantage of this culture-dependent approach is that it allows the detection of endophyte fraction missed by plating (>99%) by using polymerase chain reaction (PCR) and multiple sequencing techniques (Ma et al. 2016; Doherty et al. 2017). The main drawbacks of this approach are that it does not recover the entire microbial strains (Srivastava et al. 2019) and that the use of low specific primers could interfere with the amplification process (Mefteh et al. 2019). The combination of these two methods for endophytic isolation, therefore, gave a broad comprehension of the endophytic diversity within host plants (Maropola et al. 2015; Santoyo et al. 2016, Mefteh et al. 2019).

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8.6 Plant Growth-Promoting Mechanisms The mechanisms employed by soil bacteria and mycorrhizal (AM) fungi to enhance plant growth have been well studied (Glick 2012; Pereira and Castro 2014; Vimal et al. 2017). These microbes may affect plant growth either directly or indirectly (Fig. 8.4) (Paungfoo-Lonhienne et al. 2014; Gond et al. 2015). a. Direct plant growth promotion Endophytic bacteria and fungi possess direct plant growth-promoting potentials through, improving nutrient acquisition or mobilization, regulating or producing phytohormones, and through enhancing the antioxidant system, etc. (Vardharajula et al. 2011; White et al. 2019).

Fig. 8.4 Mechanisms employed by soil bacteria and mycorrhizal (AM) fungi to enhance plant growth

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The nutrient acquisition enhancement includes typically: atmospheric nitrogen fixation, siderophores production, and phosphorus solubilization. Although, some workers have also studied the potassium and zinc solubilization (Bhatt and Maheshwari 2020). Sulphur oxidation studies have recently been observed from the nonrhizospheric bacteria (Dhiman et al. 2020). Modulation of hormone levels may entail the synthesis or regulation of one or more plant phytohormones such as auxins (Gaby and Buckley 2011; Verma et al. 2014) mostly indole acetic acid (IAA), gibberellins, and cytokinins. Some PGPB reduces ethylene levels by synthesizing 1aminocyclopropane-1-carboxylate (ACC) deaminase enzyme, which cleaves ACC, the precursor of ethylene in all higher plants (Zahir et al. 2011). Maheshwari and colleague have been reported the role of Bacillus sp. with ACC deaminase production ability and other endophytes such as Sinorhizobium meliloti bear acdS gene conferring ACC deaminase (Kumar et al. 2012; Maheshwari et al. 2015; Aeron et al. 2014).

8.6.1 Atmospheric Nitrogen Fixation Nitrogen (N) belongs to the most essential elements that are responsible for plant growth. Plants are not able to use atmospheric nitrogen directly (Santi et al. 2013). Therefore, the use of beneficial microbes is an environment-friendly technique that enhances nitrogen fixation (Gaby and Buckley 2011; Verma et al. 2014) in both leguminous and non-leguminous plants.

8.6.2 Phosphorus Solubilization Phosphorus (P) is an important nutrient for plant growth and sustainability. It is involved in several metabolic processes (Li et al. 2017). Yet, it cannot be easily assimilated by plants because of its insoluble form (Ahemad and Kibret 2014). Microbial phosphate solubilization is required to enhance phosphate availability by secreting several organic acids (Haile et al. 2016; Chauhan et al. 2017) and other mechanisms involved in P-solubilization.

8.6.3 Siderophore Production Iron is extremely necessary for plants (Curie and Mari 2017; Tsai and Schmidt 2017). The predominant iron form in nature is a ferric ion (Fe3+ ), it is only sparingly soluble, which explains the difficulty of its assimilation by plants. Microbes are the major precursors of iron uptake through specific pathways, including siderophores production (Ahemad and Kibret 2014; Ahmad et al. 2017).

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Bacterial siderophores are implicated directly by stimulating nutrient uptake and indirectly by sequestering Fe3+ in the areas around the roots, to prevent its assimilation by pathogenic microorganisms and thus help in disease inhibition (Hayat et al. 2010).

8.6.4 Phytohormones Synthesis and Regulation Indole-3-acetic acid (IAA): Microbial auxin is a vital regulatory phytohormone (Kuhn et al. 2017). Synthesis of phytohormone auxin by microbes is well known for a long time ago. Also, IAA contributes to plant cell elongation by increasing cell osmosis, increasing cell permeability to water, increasing cell wall synthesis, decreasing wall pressure, and inhibiting or decaying leaves abscission (Muday et al. 2012; Mohite 2013). Tryptophan is an amino acid synthesized by beneficial microbes and acts as the major precursor of IAA (Gamalero and Glick 2015) and determines the induced and constitutive nature of IAA in various microorganisms. Cytokinins (CKs): Cytokinins (CKs) are compounds with a structure resembling adenine (Sakakibara et al. 2006). Their name comes from their capacity of cytokinesis or plants mitosis enhancement. Cytokinins are synthesized by plants, and several soil microorganisms (Dodd et al. 2003). Cytokine mediating-beneficial microbes act as plant growth promotors and biotic and abiotic stress inhibitors by producing or altering CKs homeostasis (O’Brien and Benkova 2013; Ritika and Mohinder 2016; Großkinsky et al. 2016). Gibberellins: The phytohormone gibberellin has an important effect on host plant development as it could regulate numerous biological processes, starting from cell division, elongation, and differentiation to fruit development and senescence (Bueso et al. 2016). Gibberellic acid (GA), is the main gibberellin product. GA producing PGPRs act by regulating GA levels in plants by increasing root surface and length (Sharma and Kaur 2018; Khan et al. 2018) and enhance plant growth and development. Abscisic Acid (ABA): Abscisic acid (ABA) is a critical plant stress hormone (Sah et al. 2016). It is responsible for the regulation of various physiological processes in stressed plants, such as limiting seed germination, inhibiting the growth of shoots and roots, and stomatal sealing (Cohen et al. 2015). PGPM’s ability to alter ABA levels in plants suggests their importance in influencing plant growth and abiotic stress resistance (Dodd et al. 2003). Jasmonic acid (JA): Being a signal molecule, jasmonic acid (JA) responds to wound and pathogenesis attacks, by upholding secondary metabolites production in plants (Gu et al. 2012; Du et al. 2013). It also increases the abundances of bacterial populations, having phytopathogens, and insects suppressive abilities (Carvalhais et al. 2013). Additionally, plants under pathogenic attack may evolve mechanisms to recruit symbionts that synthesize JA to enhance their tolerance to both the biotic and abiotic stresses (Liu et al. 2017; Ahmad et al. 2017).

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Ethylene and ACC Deaminase: Ethylene is a gaseous hormone that is responsible for plant growth. The biosynthesis of ethylene starts by converting Sadenosylmethionine (SAM) to 1-aminocyclopropane-1-carboxylate (ACC) by 1aminocyclopropane-1-carboxylate synthase (ACS) enzyme. Ethylene level gets elevated when exposed to stress conditions, resulting in reducing plant growth (Hardoim et al. 2008). In this case, bacteria could interfere by sequestering plant ACC and breaking it down into ammonia and α-ketobutyrate, thus reducing ethylene negative effect, enhancing plant stress resistance, and plant development (Naveed et al. 2014; Noumavo et al. 2016). b. Indirect plant growth promotion Bacterial indirect plant growth promotion is achieved by limiting abiotic stresses or preventing the deleterious effects of pathogenic organisms, via (i) biological control of pathogens (producing inhibitory allelochemicals, antibiotics, and cell walldegrading enzymes), (ii) parasitism, (iii) competition for niches and bioavailable nutrients, (iv) signal interference (quorum sensing), (v) volatile compounds synthesis (VOCs), and (vi) inducing systemic resistance (ISR) (Glick 2012; Alvin et al. 2014; Sheoran et al. 2015).

8.6.5 Production of Cell Wall-Degrading Enzymes Microbial cell wall-degrading enzymes play a major role in host plant protection from biotic stresses (Goswami et al. 2016). Extracellular enzymes produced by endophytic strains include chitinases, dehydrogenases, β-glucanases, amylases, cellulases, lipases, etc. (Gupta et al. 2015). Both chitinase and β-glucanase are effective in inhibiting the proliferation of hyphal by lysis and detangling of mycelia and other morphologies of fungal pathogens (Vejan et al. 2016).

8.6.6 Hydrogen Cyanide Production (HCN) Volatile compounds production include hydrogen cyanide (HCN), aldehydes, alcohols, ketones, etc. (Ulloa-Ogaz et al. 2015). Particularly, HCN is a key factor of disease proliferation (Ramette et al. 2003), since cyanide is a metabolic inhibitor that acts by protecting plants from colonization or competition (Passari et al. 2016).

8.6.7 Volatile Organic Compounds (VOCs) The low molecular weight volatile organic compounds (VOCs) involve phenylpropanoids, terpenoids, and fatty acid derivatives, they are endowed with

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antipathogenic and plant growth capacities. The endophytic bacteria act as biocontrol agents that synthesize VOCs as a part of their metabolism (Liu and Zhang 2015). VOCs pass freely through biological membranes and may be released into the soil or the atmosphere (Cappellari et al. 2019).

8.6.8 Competition for Space and Nutrients The rhizospheric soil is very rich in carbon. Therefore, it represents a source of attraction to diverse microbes, including phytopathogens (Ramamoorthy et al. 2001). Biological control agents occupy similar niches as pathogens and gradually outcompete them for occupancy (Handelsman and Stabb 1996) and “precious” nutrients, leading to a reduction in nutrient availability to phytopathogens (Thakur and Singh 2018).

8.6.9 Antibiosis and Antibiotics Antibiosis is a mechanism by which the biocontrol agent produces several secondary metabolites to inhibit or suppress pathogens (Haas and Défago 2005). Antibiotics production is the main biocontrol mechanism employed by a variety of antagonistic microbes in the rhizosphere. They are defined as a group of low-molecular weight organic compounds that are effective in suppressing bacterial growth (Glick et al. 2007).

8.6.10 Detoxification and Degradation of Pathogens Virulence Factors Microbial pathogens could produce toxins aiming at inhibiting antagonistic microorganisms. Moreover, it was recently demonstrated that certain beneficial bacteria could attenuate pathogen quorum-sensing abilities. Thus, they block virulence genes expression, because bacterial phytopathogens require series of quorum-sensing signals to activate their virulence factors (von Bodman et al. 2003).

8.6.11 Induced Systemic Resistance (ISR) Induced systemic resistance (ISR) is a defense mechanism enhanced by microbial endophytes to enhance the plant’s protective levels against a wide range of pathogens

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(Alvin et al. 2014). ISR activation majorly occurs through the SA-independent pathway involving jasmonate and ethylene signals (Pettersson and Baath 2004). They increase the sensitivity to these hormones, to activate several defense genes (Hase et al. 2003).

8.7 Biological Applications of Endophytic Microorganisms Nowadays, endophytic microorganisms have been used in multiple fields as biological alternatives to chemical compounds. These microbial populations were involved in biocontrol of phytopathogens, plant growth stimulation, phytoremediation, bioremediation, medicinal and industrial applications (Strobel and Daisy 2003; Schulz 2006; Jalgaonwala et al. 2011; Godstime et al. 2014; Shukla et al. 2014; Chaudhry et al. 2017; Uzma et al. 2018). a. Biological control Biological control or Biocontrol is the use of microbial antagonists to manage or inhibit plant pathogens (bacteria, fungi, viruses, and nematodes) (Mehta et al. 2014). This environment-friendly approach may be an effective solution to get rid of chemical pesticides in the agricultural sector. Therefore, the bioformulation of beneficial microorganisms could help in enhancing and maintaining plant productivity naturally and cost-effectively (Guédez et al. 2008; Griffin 2014; Nion and Toyota 2015; Kergunteuil et al. 2016; Alenezi et al. 2017; Høyer et al. 2019). b. Bioremediation Bioremediation process implies the use of microbial populations to remove or lessen pollutants (heavy metals, dye, organic compounds, crude oil, etc.) toxicity from the biosphere (Kinoshita et al. 2008; Zhou et al. 2014; Limcharoensuk et al. 2015; Govarthanan et al. 2016; Ijaz et al. 2016; Bharagava et al. 2017; Mefteh et al. 2019). It is achieved through two major mechanisms: biosorption which is one of the most convenient techniques of sequestration. It binds contaminants onto the cell walls of microorganisms (Kousha et al. 2012; Bera et al. 2016; Chew and Ting 2016; Ting et al. 2016) and bioaccumulation consisting of transporting and precipitating toxic elements into microbial cells (Kiran et al. 2017) and transforming them into non-toxic forms (Sathish et al. 2012; Sim et al. 2018, 2019). c. Phytoremediation The association of plant-microbes is a perfect combination to solve environmental pollution/contamination in a maintained, cost-effective, and environment-friendly manner (Glick 2010; Shin et al. 2012; Chen et al. 2014; Dharni et al. 2014; Ma et al. 2015; Chirakkara et al. 2016, Rekik et al. 2017; Mefteh et al. 2019). Recently, heavy metal removal/alleviation by endophytes has been highly studied (Weyens et al. 2009; Luo et al. 2011; Langella et al. 2014), it is achieved via multiple methods

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including metal precipitation, biodegradation, biotransformation, bioaccumulation, and sequestration (Zhu et al. 2014; Babu et al. 2015). d. Medicinal application Medicinal plants constitute a reservoir of tremendous bioactive metabolites used for disease treatments from ancient times (Paramanantham et al. 2019). During the last few decades, researchers have discovered several interesting medicinal/pharmaceutical drugs and antibiotics originating from diverse endophytic microbes living inside medicinal and non-medicinal plants. They have inherent potentials to produce bioactive metabolic compounds possessing therapeutic properties to treat numerous infections and diseases (Kusari et al. 2014) such as cancer, diabetic, microbial, fungal, and viral diseases (Strobel and Daisy 2003; Huang et al. 2007; Yu et al. 2010; Kharwar et al. 2011; Akone et al. 2016; Mefteh et al. 2017; Venieraki et al. 2017). Singh and Dubey (2015) reported that natural compounds originating from the medicinal plants-endophytes association, constitute above 50% of natural products in the market and this was further confirmed by Passari et al. (2017). The same endophytic strain isolated from several medicinal plants could produce diverse biological activities through the production of several medicinal compounds (Tan and Zou 2001; Khiralla et al. 2017).

8.8 Omic Approaches for Endophytes Traditional methods used to identify and characterize endophytic microbes were supported by in silico approaches which help in understanding the functional potentialities of endophytes (Gianoulis et al. 2012; Nicolas et al. 2014; Chetia et al. 2019). The number of microbial omic studies have been developed rapidly in the recent years due to the next generation sequencing (NGS) methods which are increasingly lowering their costs (Kodama et al. 2011; Kaul et al. 2016; Belbahri et al. 2017; Slama et al. 2018; Cheffi et al. 2019). Nowadays, there is a large amount of whole bacterial and fungal genomes that have been sequenced and stored in several open-access databases and platforms (Figs. 8.5 and 8.6). The combination of omic approaches (genomic, transcriptomic, metabolomics, and proteomics) allowed exploration of endophytes potentials and their interactions with hosts. In fact, (i) genomic is the technology of total genome sequencing of microorganisms (Campisano et al. 2014; Akinsanya et al. 2015; Belbahri et al. 2017; Sengupta et al. 2017; Correa-Galeote et al. 2018), (ii) transcriptomic studies provide instructions about gene status (AguiarPulido et al. 2016), (iii) metabolomic allow identification of novel secondary metabolites exhibited by microbes (Rasmussen et al. 2011; Chetia et al. 2019), (iv) lastly proteomic is a multivariate technology of endophytic proteins expression (Kaul et al. 2016; Peng et al. 2019).

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Fig. 8.5 Pie-chart of endophytic bacteria community based on whole genome

8.9 Conclusion and Prospects While endophytes have been known for more than a century, they only recently found their way to applied research. Present applications include diverse fields including agriculture, medicine, industry, pharmacology, bio, and phytoremediation. It has been proven that endophytes could be more reliable and low-cost sources of natural drugs than chemical compounds because of their intimate associations with plants and their non-harmful effects on the environment. In the prospects, it is essential to understand the mechanisms interfering in plant–endophytes and endophyte–endophyte

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Fig. 8.6 Pie-chart of endophytic fungal community based on whole genome

interactions to accomplish all biotechnological applications. Additionally, further research in emerging “omic” technologies involving transcriptomics, metagenomics, and metatranscriptomics approaches predict discoveries that will unravel plant–endophytes relationships and will strengthen the potential use of endophytes in applied research. Microbial secretomes and volatiles are also widely investigated. It is estimated that the genomic and metabolic data mining will ultimately provide new insights into their successful implementation in all the above discussed fields.

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Chapter 9

Phosphate Solubilization by Endophytes from the Tropical Plants Paulo Teixeira Lacava, Paula Cristiane Machado, and Paulo Henrique Marques de Andrade

Abstract Currently, agriculture depends heavily on a variety of agrochemicals, such as mineral fertilizers and pesticides, that often have adverse effects on human health and environmental ecosystems. Furthermore, the indiscriminate application of pesticides has severe effects on soil ecology that may lead to alterations in plant and soil microbiomes. Modern agricultural biotechnology has shown that microbial inoculants can be used to enhance plant growth and can thereby reduce the use of agrochemicals. In this context, the utilization of endophytic microorganisms for agricultural purposes has increased recently, especially their use for plant growth promotion. Endophytes are microorganisms that live in plant tissues without causing apparent disease in the host plant. Endophytic microorganisms promote plant growth in three major ways: they synthesize particular compounds that are useful for the plants, they facilitate the uptake of certain nutrients from the soil, and they control or prevent diseases. Growth promotion mediated by endophytes occurs via several mechanisms: the production of vital enzymes; the production of hormones such as auxin (indoleacetic acid [IAA]); the symbiotic fixation of nitrogen; the production of siderophores, chitinases, or antibiotics for protection from phytopathogens; and the solubilization and mineralization of nutrients, particularly insoluble mineral phosphates. Endophytic microorganisms can be used to improve nutrient utilization because they solubilize phosphate, making it available for absorption by plants. Among these microorganisms are phosphate-solubilizing bacteria and fungi that P. T. Lacava (B) · P. H. M. de Andrade Laboratory of Microbiology and Biomolecules – LaMiB, Department of Morphology and Pathology, Center for Biological and Health Sciences, Federal University of São Carlos, Via Washington Luís km 235, PO BOX 676, São Carlos, SP 13565-905, Brazil e-mail: [email protected] P. T. Lacava · P. C. Machado Biotechnology Graduation Program – PPGBiotec, Center of Exact Sciences and Technology, Federal University of São Carlos, Via Washington Luís km 235, São Carlos, SP 13565-905, Brazil P. T. Lacava · P. H. M. de Andrade Evolutionary Genetics and Molecular Biology Graduation Program – PPGGEv, Center for Biological and Health Sciences, Federal University of São Carlos, Via Washington Luís km 235, São Carlos, SP 13565-905, Brazil © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_9

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participate in the phosphorus cycle and facilitate the conversion of insoluble P to soluble forms via the secretion of organic acids and phosphatases. In this way, they make P available to the plant. Over the past two decades, much information on the role of endophytes in nature has been collected. Their ability to colonize internal host tissues has made endophytes valuable as a tool for improving crop performance. Most studies on endophytes have been carried out using hosts from temperate countries, but data from tropical regions remain scarce. Tropical plants host a great diversity of endophytic microorganisms, many of which are not yet classified and possibly belong to new genera and species. In this chapter, we focus on examples of endophytic microorganisms, especially those that have the potential to promote plant growth through phosphate solubilization. Keywords Biofertilizers · Endophytic microbes · Phosphate solubilization · Plant growth promotion · Sustainable agriculture

9.1 Introduction The significance of endophytic microorganisms for agricultural purposes has increased recently, especially their use for pest and disease control (biological control) and plant growth promotion (Vyas and Bansal 2018; Maheshwari and Annapurna 2017; Gautam and Avasthi 2019). Endophytes promote plant growth in many ways, such as by producing enzymes and hormones and acting against phytopathogens via the production of siderophores, chitinolytic enzymes, or antibiotics; and solubilizing nutrients such as phosphates (Azevedo and Quecine 2019). A large number of macronutrients and other minerals are required for the balanced growth of the plants. One of them is Phosphorus. Phosphorus which promotes root development, tillering, and early flowering and has a role in other functions such as metabolic activities, particularly protein synthesis (Tanwar and Shaktawat 2003). Phosphorus in soil is present in both inorganic and organic insoluble forms. Phosphate solubilization by endophytes is an interesting component of plant growth promotion because endophytic bacteria are compatible with host plants and can colonize the tissues of host plants without being identified as phytopathogens (Rosenblueth and Martínez-Romero 2006). The interactions between endophytes and plants can promote plant health and play a significant role in low-input sustainable agriculture for both food and nonfood crops (Rai et al. 2014; Golinska et al. 2015). In the past two decades, large number of publications have appeared on the role of endophytic microorganisms in nature (Azevedo and Quecine 2019). The ability of endophytes to colonize internal host plant tissues has made them valuable as a tool for improving crop performance (Araújo et al. 2008). The exploration of endophytes in unstudied hosts, such as tropical plants, is important for assessing the potential of these microorganisms in different application areas and for identifying natural compounds that could be used in agriculture

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and biotechnology (Golinska et al. 2015). Still a large number of plants have yet to be investigated.

9.2 Phosphorus Solubilization by Microorganisms Phosphorus (P) is one of the major growth-limiting macronutrients required for proper plant growth, particularly in tropical areas (Santana et al. 2016). Based on the availability of P to plants, the different forms of P can be categorized as soluble P and insoluble P. The soluble form is easily available for uptake by plants. In contrast, an insoluble form is very stable in soil and persists in an unavailable form (Ahemad et al. 2009). Inspite of its abundance in soil and therefore cannot support the plant growth due to its unavailability. Moreover, almost 75% of phosphorus applied as fertilizer forms complexes with soil and becomes unavailable for the plants (Ezawa et al. 2002). More details about the identification of the major processes of the soil P cycle that affect soil solution P concentrations as dissolution–precipitation, sorption desorption, and mineralization–immobilization (biologically mediated conversions of P between inorganic and organic forms) are presented in a review by Sims and Pierzynski (2005) and other publications. Microorganisms play an important role in all three major components of the soil P cycle such as (1) release of complexing or mineral dissolving compounds, e.g., organic acid anions, siderophores, protons, hydroxyl ions, CO2 , (2) liberation of extracellular enzymes (biochemical P mineralization), and (3) the release of P during substrate degradation (biological P mineralization) (Sharma et al 2013). Some bacterial species have mineralization and solubilization potential for organic and inorganic phosphorus, respectively (Hilda and Fraga 2000; Khiari and Parent 2005). Phosphorus solubilizing activity is determined by the ability of microbes to release metabolites such as organic acids, which through their hydroxyl and carboxyl groups chelate the cation bound to phosphate, the latter being converted to soluble forms (Sagoe et al. 1998).

9.3 Endophytic Microorganisms: A Way to Reduce the Application of Agrochemicals in Agrobiology Systems Agriculture is anti-ecological by nature, and the large-scale use of chemical fertilizers, insecticides, fungicides, herbicides, and antibiotics has led to profound biological changes. The increasing use of fertilizers and highly productive systems has also created environmental problems such as the deterioration of soil quality, surface water, and groundwater, as well as air pollution, reduced biodiversity, and suppressed ecosystem function (Vance 2001). Additionally, chemical pesticides and fertilizers

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can cause significant damage to ecosystems through the processes of bioaccumulation and biomagnification due to their synthetic nature (Sarbadhikary and Mandal 2018). Consequently, interest in the development of new strategies to achieve more sustainable agricultural practices has increased significantly in recent years (Azevedo and Quecine 2019). In this context, biofertilizers are an interesting alternative to the use of agrochemicals, as biofertilizers may be a safe substitute for agrochemicals that would greatly minimize ecological disturbance from agriculture. Biofertilizers are low-cost, eco-friendly tools, and their persistent use increases soil health and fertility (Ngamau et al. 2014). In this context, there is renewed scientific and commercial interest in the use of endophytic microorganisms as biofertilizers because of their potential to improve plant quality and growth and their close association with internal tissues of the host plant (Schulz et al. 1998, 1999; Ngamau et al. 2014). Biofertilizers can improve crop health by fixing nitrogen (Islam et al. 2013), solubilizing phosphate (Ghosh et al. 2016), or promoting plant growth by producing plant growth-promoting factors such as auxin (IAA) and gibberellins (Kang et al. 2014; Reetha et al. 2014). Plant growth-promoting rhizobacteria (Vessey 2003) and vesicular-arbuscular mycorrhizae (Abbasi et al. 2015) are the microorganisms that are used most often as biofertilizers. Recently, many researchers have also reported the use of endophytic microorganisms in agricultural fields for crop improvement (Ngamau et al. 2014). The term endophyte is applied to microorganisms that live within plant tissues for all or part of their life cycles and cause no apparent infections or symptoms of a disease (Strobel et al. 2004). Hallmann et al. (1997) described endophytes as organisms that can be isolated from surface-sterilized plant parts or extracted from inner tissues and that cause no damage to the host plant. Also, Azevedo and Araújo (2007) suggested that endophytes are all microorganisms, whether culturable or not, that inhabit the interior of plant tissues, cause no harm to the host, and do not develop external structures. Endophytes have an intimate interaction with plants and are capable of promoting plant growth. The use of these microorganisms at certain stages of agricultural production can lead to a significant increase in productivity or a reduction in inputs such as nitrogen and phosphate fertilizers (Malboobi et al. 2009; Rukshana-Begum and Tamilselvi 2016). The plant growth-promoting effects of endophytes include increased plant height and biomass in shoots, stems, and roots; formation of leaf and root hairs; lignification of the xylem vessels; and increased crop yield, as the ability of endophytes to stimulate plant growth has been attributed to mechanisms such as phytohormone production and phosphate solubilization (Ahmad et al. 2008). Some soil microorganisms solubilize the unavailable forms of inorganic P in the soil (Son et al. 2006; Chai et al. 2011), and recent studies have confirmed that endophytic microorganisms also possess this capacity (Vitorino et al 2012). After nitrogen, phosphorus (P) is the second most limiting nutrient for plant development. It is only taken up in monobasic or dibasic soluble forms (Zaidi et al. 2006). Phosphorus constitutes 0.2% of plant dry weight and is a structural component of macromolecules such as nucleic acids, phospholipids, and adenosine triphosphate (ATP) (Martins 2004). Phosphorus is an essential element for the establishment and

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development of plants because it improves the entire root system, which consequently improves the shoot (Raven et al. 2001). However, phosphates applied to agricultural soils are rapidly immobilized and rendered inaccessible to plants. Due to this rapid immobilization, many agricultural soils have large reservoirs of phosphates in inaccessible forms (Rodríguez and Fraga 1999; Rodríguez et al. 2006). In this scenario, the ability of microorganisms to solubilize phosphorus is determined by their ability to release metabolites such as organic acids, which chelate the cation bound to the phosphate through their hydroxyl and carboxyl groups, converting the inaccessible phosphate to a soluble form (van der Heijden et al. 2008). Even in a phosphorus-rich soil, only a small fraction of the phosphorous is available to plants because most of it is found in insoluble forms, and plants are not able to absorb it (Gyaneshwar et al. 2002). Some kinds of the microorganism may be used to improve plant nutrient utilization because they solubilize phosphate, making it available for absorption by the plant. Among these microorganisms are phosphate-solubilizing bacteria and fungi that participate in the phosphorus cycle and facilitate the conversion of insoluble phosphorus to soluble forms via the secretion of organic acids and phosphatases, thus making phosphorus available to the plant (Oliveira et al. 2003). Besides, phosphatesolubilizing microorganisms could play an important role in supplying phosphate to plants in an eco-friendly and sustainable way (Oliveira et al. 2009; Gomes et al. 2014). Phosphate-solubilizing microorganisms are found in soil, especially in rhizospheric microbial populations, and their numbers vary depending on the type of soil (Mohammadi 2012). These microorganisms release low molecular-weight organic acids that solubilize mineral phosphates and reduce the pH of the soil (Pérez et al. 2007; Gomes et al. 2014). Additionally, they have been widely tested as biofertilizers and inoculants to increase crop yield through phosphate solubilization (Karpagam and Nagalakshmi 2014; Baliah et al. 2016; Gurikar et al. 2016). Endophytes represent a group of microorganisms that can colonize plants without inducing the host defense pathway (Azevedo et al. 2000). Thus, the distinction between free-living soil microorganisms, the rhizosphere population, and the symbionts of a host plant may represent a true continuum, with microbes able to move between the soil, the rhizosphere, and the inside of the plant as endophytes (Farrar et al. 2014; de Abreu et al 2017). In this case, several species of Bacillus and Pseudomonas use nutrient niches in the rhizosphere and change from a freeliving condition to an endophytic state (Rosenblueth and Martínez-Romero 2006; Gaiero et al. 2013). In this way, endophytes can be transported from the seeds into the roots and tissues, reducing the need for continuous inoculation (Johnston-Monje and Raizada 2011). However, the ability of endophytic microorganisms to solubilize phosphates in tropical and subtropical soils has not been sufficiently studied (de Abreu et al. 2017). Endophytes, as phosphate solubilizers, are more competitive than free-living or facultative microorganisms inside the host plant since the endophyte– plant interaction is the result of an evolutionary process that is controlled by genes of both organisms (Rosenblueth and Martínez-Romero 2006). Endophytes can increase the availability of P for the plants by solubilizing precipitated phosphates, using mechanisms like acidification, chelation, ion exchange, and

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production of organic acids (Nautiyal et al. 2000). They can also increase P availability in the soil by secreting acid phosphatase that can mineralize organic phosphorus (van der Heijden et al. 2008). Moreover, these microorganisms can prevent phosphate adsorption and fixation under phosphate-limiting conditions by assimilating solubilized P (Khan and Joergensen 2009). In a recent review presented by Afzal et al. (2019), they discussed the role of plant beneficial endophytic bacteria with special reference to phosphate solubilization as commonly found in PGPR. For instance, around 59–100% of endophytic populations from cactus, strawberry, sunflower, soybean, and other legumes proved to be mineral phosphate solubilizers (Dias et al. 2009a; Forchetti et al. 2007; Kuklinsky-Sobral et al. 2004; Palaniappan et al. 2010; Puente et al. 2009).

9.4 Endophytic Bacteria from Tropical Plants of Economic Importance: Phosphorus Solubilization Potential 9.4.1 Endophytic Bacteria from Coffea arabica Similar to the free living bacteria and rhizobia, the endophytes generally influence the plant for their growth and development. These bacteria have potential to exhibit their effects in order to benefit the plants in a befitting manner. Some of them are given below. Coffee (Coffea arabica L.) is a perennial plant widely cultivated in many tropical countries. It belongs to the family Rubiaceae, which has approximately 500 genera and more than 6,000 species. It is the most important genus in economic terms, mainly due to coffee production used as beverage (Mendes et al. 1995). Due to its continental dimensions, Brazil has a variety of climatic conditions, reliefs, altitudes, and latitudes. Such bio-geography allows for the production of many types and qualities of coffee, including specialty coffees and organic coffee, whose consumption has increased as society has begun to question the sustainability of the current conventional agricultural model (Brasil 2015). The microbiota associated with coffee plants may play a critical role in coffee quality. However, the microbial diversity and agricultural potential associated with coffee plants are still poorly characterized. There are some examples of studies of microorganisms associated with coffee, such as Muleta et al. (2013), who reported phosphate-solubilizing rhizobacteria associated with Coffea arabica L. in the natural coffee forests of southwestern Ethiopia. In this study, a total of 395 rhizobacterial isolates tested for P solubilization formed visible dissolution haloes on the Pikovskaya’s agar (PA) culture. According to these authors, two Erwinia species and a Pseudomonas chlororaphis produced the highest solubilization index, and the production of organic acids by these coffee-associated strains could be considered the major mechanism involved in the solubilization of insoluble hydroxyapatite/tricalcium. Earlier, Musson (1994) suggested that endophytes can act as efficient growth promoters, probably in the same manner as rhizobacteria, by producing

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hormones and other growth factors. Additionally, bio-priming and seed coating appeared as an efficient method in growth-promotion because endophytes as organisms can be adhered onto the seed surface (Rosenblueth and Martínez-Romero 2006; Ryan et al. 2008). The endophytic microbiota plays a role not only in supplying plants with the basic nutrients that are indispensable for their growth but also in the mechanisms of adaptation to various environmental stresses, important in terms of crop yields (Ku´zniar et al. 2019). The rational method of plant growth promotion by endophytes is the improvement of plant nutrient acquisition. However, the mechanisms for direct nutrient transfer from endophytic bacteria to plants have been elusive (Pandey et al. 2018; Roley et al. 2018). In some cases, endophytes have been shown to increase the solubilization of bound phosphates in the rhizosphere and thus have been hypothesized to function by increasing the plant phosphate supply in the rhizosphere for its uptake by plants(Shehata et al. 2017). In a recent publication, White et al. (2018) proposed that many host plants acquire some nutrients directly from symbiotic microbes by a process called the ‘rhizophagy cycle’. In this cycle, symbiotic microbes alternate between an endophytic phase and a free-living soil phase. The authors hypothesize that microbes acquire soil nutrients in the free-living soil phase and that those nutrients are extracted from microbes oxidatively in the intracellular/endophytic phase. In this review, White et al. (2018) discuss the proposed mechanisms that plants employ to manipulate symbiotic microbes to transport nutrients from the soil into root cell periplasmic spaces. Oliveira et al (2013) investigated endophytic diversity in Coffea arabica L. cherries from southeastern Brazil by using culture-independent approaches to identify the associated microorganisms with the goal of better understanding their ecology and potential role in determining coffee quality. In our research group, we isolated endophytic bacteria from coffee cherries (Fig. 9.1), and identification by 16S rRNA genes and fatty acid methyl esters (FAMEs) revealed 3 major genera: Bacillus agaradhaerens, Paenibacillus sp.; and Pantoea agglomerans. According to Oliveira et al. (2013), the bacterial sequences showing high similarity with cultured and uncultured

Fig. 9.1 Endophytic bacteria isolated from Coffea arabica L. cherries. Details of endophytic growth indicated by black arrows (Photo credit: Corresponding Author)

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bacteria belonged to the Betaproteobacteria, Gammaproteobacteria, and Firmicutes phyla. Phylogenetic analyses of cloned sequences from Firmicutes revealed that most sequences fell into 3 major genera: Bacillus, Staphylococcus, and Paenibacillus. In this case, we found similar results to those reported by Oliveira et al. (2013) regarding the diversity of endophytic bacteria isolated from C. arabica L. cherries. Silva et al. (2012) reported the potential of endophytic bacteria isolated from healthy Coffea arabica L. and Coffea robusta L. from Pedreira, Mococa, and Pindorama counties, State of São Paulo, Brazil. Previously, promising growthpromoter endophytic strains were evaluated qualitatively in vitro for the production of phosphatase, indole acetic acid (IAA), siderophores, cytokinins, and gibberellins (CYT/GIB). A total of two hundred seventeen strains were evaluated for their potential to promote the growth of coffee seedlings in vivo. According to the authors (Silva et al. 2012), the growth-promoting indexes of 119 bacterial strains were higher than those of the control. Additionally, the Scott–Knott cluster test indicated that the indexes of six bacterial strains, 85G (Escherichia fergusonii), 161G, 163G, 160G, 150G (Acinetobacter calcoaceticus), and 109G (Salmonella enterica), differed significantly from that of the control. However, of these six strains showed with the best performance in vivo, only two (161G and 160G) produced phosphatase as a positive plant-growth promotion parameter when tested in vitro. In our research, we have investigated the ability of endophytes from different host plants to promote plant growth, including phosphate solubilization. In this context, Andrade (2019) performed a study that included the isolation, biochemical characterization, identification, and analysis of the genetic diversity of the endophytic bacterial community associated with C. arabica L. from conventional and organic cultivation sources. The results demonstrated that 342 endophytic bacterial isolates were evaluated for in vitro growth factors, where, about 64.33% isolates were solubilized inorganic phosphate. The identification of endophytic strains was performed by bacterial cell protein analysis by matrix-assisted laser desorption/ionization-time-offlight (MALDI-TOF) and by partial sequencing of the 16S rDNA gene. The genera identified were Arthrobacter, Bacillus, Cronobacter, Enterobacter, Erwinia, Klebsiella, Kosakonia, Kurthia, Lysinibacillus, Microbacterium, Pantoea, Pseudomonas, and Rhizobium. In this case study (Andrade 2019), the endophytic strains with the best performance for in vitro growth factors, including phosphate solubilization, were selected for inoculation in coffee seedlings. Ten endophytic strains were selected based on the biochemical characterization previously performed in vitro about the potential for plant growth promotion. The treatments consisted of a control (C) with 8 replicates where the seedlings were inoculated only with PBS buffer and 10 treatments (T1 to T10) with 8 replicates which consisted of weekly inoculation of the seedlings with a bacterial suspension of CRM 162 - Erwinia bilingiae (T1); CRM 202 - Kosakonia cowanii (T2); CRA 241 Enterobacter tabaci (T3); CRA 250 Enterobacter tabaci (T4); CRA 298 - Pantoea brenneri (T5) from conventionally grown coffee; OFR 175 - Lysinibacillus mangiferihumi (T6); OFR 176-Lysinibacillus mangiferihumi (T7); OFR 164 - Klebsiella pneumoniae (T8); OFO 340 - Enterobacter bugandensis (T9); or ORM 326 - Klebsiella michiganensis (T10). A total of 180 days after the first

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Fig. 9.2 Average root system length (RL) in millimeters (mm) of 8 plants per treatment (T1 to T10), measured 180 days after the first inoculation of bacteria with the potential for plant growth promotion

inoculation, the following variables were evaluated: aerial height (AH), root length (RL), stem diameter (SD), aerial dry weight (ADW), and dry weight of the root system (DWRS). All treatments of plants inoculated, except for the T3 treatment, all caused a reduction in AH corresponding to the plants of a control group. For RL, all treatments differed significantly from the control, showing an increase in root system length of 77.76%, on an average. For the variables SD, ADW, and DWRS, and the analysis of macro- and micronutrients in the leaf tissue, it was possible to observe that none of the treatments differed significantly from the control. All statistical analyses were performed considering p ≤ 0.05. A principal component analysis showed that RL explained 99% of the total variation in the observed morphological characteristics; that is, the tested bacterial strains were able to promote the growth of the coffee seedlings (Fig. 9.2).

9.4.2 Endophytic Bacteria from Jatropha curcas Jatropha (Jatropha curcas L.), which belongs to the Euphorbiaceae family, is a plant that is genetically close to the castor plant (Ricinus communis L.); it originates from Central America and is currently distributed in all tropical regions of the globe (Kumar and Tewari 2015; Kumar et al. 2016). Jatropha cultivation has received more attention in the last few decades due to its role in biodiesel production. Jatropha is also recommended for cultivation for soil health improvement, climate change mitigation, carbon sequestration, and socio-economic development (Islam et al. 2014). The yield of jatropha varies from 0.2 kg to >2 kg seeds from a single plant or 2–12 t ha−1 (Tikkoo et al. 2013; Singh et al. 2014). In Brazil, jatropha has received special attention as an alternative supply of vegetable oil as a raw material for biodiesel manufacturing due to the biotechnological potential of its seeds (Laviola et al. 2011; 2015). Several studies on climatic adaptation and productivity have been developed on the genetic variability of jatropha (Reddy et al. 2008; Behera et al. 2010; Laviola et al. 2010;

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2012; Edrisi et al. 2015), but only a few studies in Brazil have focused on the analysis of the microbial community associated with this species (Moniruzzaman et al. 2016). Jatropha can survive with limited nutrients and under harsh environmental conditions. Planting jatropha is also recommended for pest control, bioremediation, and soil reclamation. Jatropha exhibits drought tolerance, rapid growth, easy propagation, and adaptation to a wide range of environmental stress conditions. These features make it the most popular second-generation biofuel resource (Abhilash et al. 2011). It is not clear how jatropha adapts to extreme conditions. However, Mohanty et al. (2017) hypothesize that its ability to adapt to environmental stresses could be due to its endophytes (Qin et al. 2012; Madhaiyan et al. 2013). Our research group reported the characterization of seventy-two endophytic bacteria associated with J. curcas plants that had the potential to promote plant growth. Of the tested isolates, 43% solubilized inorganic phosphate. These endophytic strains were identified by partial sequencing of the 16S rDNA gene, and the most common genera were Bacillus, Citrobacter, Curtobacterium, Enterococcus, Klebsiella, Microbacterium, Promicromonosporaceae, Sanguibacter, and Serratia (Machado 2015). Among the endophytic genera identified and acted as potential phosphate solubilizers, Bacillus, Citrobacter, Curtobacterium, Klebsiella, and Serratia showed a high phosphate solubilization index. Bacillus spp. exist as endophytes that help the host plant in different ways, one of which is supplying soluble phosphorus by solubilizing phosphorous (Kang et al. 2014; Pérez-García et al. 2011). Andrade (2012) reported six different species of Bacillus sp. that were capable of solubilizing calcium phosphate, with solubilization indexes varying from 0.42 to 2.28 cm. Dias et al. (2009b) analyzed endophytes isolated from strawberry, mainly Bacillus subtilis and B. megaterium, both of which were able to solubilize phosphate. In vitro phosphate solubilization activity has also been documented in Citrobacter sp. strains; this genus belongs to the Enterobacteriaceae family (Kämpfer 2003). In studies conducted by Reginatto (2008), a strain of Citrobacter werkmanni with the ability to solubilize phosphate was endophytically isolated from Vriesea friburgensis. Recently, Machado (2019) reported on the inoculation in corn seeds of eight endophytic bacterial strains consisted of a control (C1) containing only TSB culture medium and the application of bacterial suspensions of EPM-2 Serratia sp. strain (T1), EPM-4 Klebsiella sp. strain (T2), EPM-34 Curtobacterium sp. strain (T3), EPM-41A Bacillus sp. strain (T4), EPM-54 Bacillus sp. strain (T5), EPM-63 Klebsiella sp. strain (T6), EPM-63B Citrobacter sp. strain (T7) and EPM-92 Bacillus sp. strain (T8). Need-based irrigation was carried out, the plants were grown in a greenhouse, and Hoagland and Arnon (1950) nutrient solution was added to the plants after 30 and 60 days of the experiment. At 30 and 60 days after sowing, the plant vegetative parameters such as: shoot height (APA), shoot diameter (DM), shoot dry weight (PSPA), and dry weight of the root system were examined. In the evaluations performed at 30 and 60 days, it was observed that for the variable APA, none of the treatments differed significantly from each other; however, the control presented a significant difference in stem diameter from the other treatments. The DM value of the control treatment was greater than those of the other treatments, and at the 60-day

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evaluation, the dry weight of the aerial part (PSPA) and the dry weight of the root system (PSSR), in the control treatment were higher than those in the other treatments. Among the treatments inoculated with endophytic strains, the T1 treatment (EPM2- Serratia marcescens) exhibited significantly higher values for all growth parameters in comparison to other treatments (Unpublished data). Recently, Mohanty et al. (2017 characterized the endophytic bacteria of J. curcas and evaluated their plant growth-promoting effect on maize (Zea mays L.). Fifteen isolates were sequenced by their 16S rRNA genes and characterized based on their carbon source utilization and plant growth-promoting activities. The main genera found were Brevibacillus, Paenibacillus, Rhizobium, and Sphingomonas. These strains preferred to grow on methanol, ethanol, glucose, fructose, sucrose, and gelatin and these strains exhibited catalase, nitrate reductase, ACC deaminase, and phosphatase activities. All isolates were positive for phosphate and IAA production. Inoculation of the endophytic strains on maize seeds significantly increased the shoot and root length of seedlings compared with those of noninoculated seedlings. Potassium solubilization is important for K-assimilation. The phosphatase activity of endophytic bacteria and its relationship to plant growth promotion is interesting. The authors presumed P-mineralization in the rhizosphere by the enzymatic reaction carried by root-tissue exudates containing phosphatases, was also postulated.

9.4.3 Plant Growth-Promoting Potential of Phosphate Solubilization by Endophytic Bacteria Isolated from Tropical Mangrove Forests Mangroves are typical tropical ecosystems situated between the land and the sea. These biological communities are frequently found in tropical and subtropical areas and occupy approximately 18.1 million hectares of the planet. These ecosystems demand high nutrient availability at the start of the trophic chain, which confers high importance on the activities of microorganisms, such as bacteria, that are responsible for the processes of degradation and formation of essential compounds and most of the carbon flow in the sediments of mangrove forests (Holguin et al. 2001). The adaptation of bacterial species to mangrove conditions indicates a potential source of biotechnological resources to be explored, including the discovery of new bacterial species that produce organic acids and enzymes that can be used for agriculture and industry (Dias et al. 2009b). In this scenario, endophytic bacteria are of agronomic interest because these organisms can enhance plant growth and improve plant nutrition through diverse mechanisms such as phosphorus solubilization (Quecine et al. 2014; Rukshana-Begum and Tamilselvi 2016). Gayathri et al. (2010) isolated endophytic bacteria from the healthy leaves of mangrove species from the Pichavaram mangrove forest in Tamil Nadu, India. In total, 104 endophytic bacteria only six endophytic isolates showed phosphate solubilization activity. This study demonstrated that mangroves are sources of endophytic

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bacteria with the potential for phosphate solubilization. Janarthine and Eganathan (2012) isolated endophytic bacteria from surface-sterilized pneumatophores of Avicennia marina, a plant common to all mangroves of India. Among 13 endophytic bacteria, four isolates were genotypically identified as Bacillus spp., B. cereus, Enterobacter sp., and Sporosarcina aquimarina. The potential of the endophytic strain S. aquimarina SjAM16103 to promote plant growth was analyzed in vitro and in vivo. The results indicated that SjAM16103 produced 2.37 µmol/mL IAA, siderophores and was able to solubilize insoluble phosphate. Gayathri and Muralikrishnan (2013), observed that 24 endophytic bacteria exhibited phosphate solubilization in vitro according to the method described by Pandey et al. (2008). Tam et al. (2018) reported the isolation of P- solubilizing endophytic bacteria associated with Rhizophora mucronate and Avicennia alba, naturally growing mangrove species. The inorganic phosphate solubilizing ability by endophytes was tested on the National Botanical Research Institute’s phosphate (NBRIP) medium and the P2 O5 concentration was measured by the ammonium molybdate method (Nautiyal et al. 2000). All 86 endophytic isolates grew well on the NBRIP medium showed phosphate solubilization abilities. Brazilian mangroves are primarily made up of three tree species, Rhizophora mangle, Laguncularia racemosa, and Avicennia sp. (Dias et al. 2009b), from which several diverse endophytic bacteria (Castro et al. 2014) have been isolated. Our research group evaluated a large number of endophytic bacterial strains, from three different plant species, namely, R. mangle, L. racemosa, and Avicennia sp., to examine phosphate solubilization (Castro et al. 2018). All 115 strains examined produced a halo during the phosphate solubilization test in vitro. The endophytic strain MCR1.48 (Enterobacter sp.), which has a high P solubilization index, was selected for in vivo assays in Acacia polyphylla. We selected the commonly used reforestation tree A. polyphylla, which has few published studies involving inoculation by bacteria of agronomic interest and used for the reforestation of degraded areas in Brazil and reflects the ability of this leguminous tree species to recover degraded soils, thereby decreasing costs and increasing benefits to the environment (Rao et al. 2007). Inoculation with Enterobacter sp. strain MCR1.48 increased the dry mass of A. polyphylla shoots and roots, suggesting that the presence of the endophyte generates important benefits that promote the growth and fitness of this plant. In this context, Castro et al. (2018) reported that the inoculation of a highly P-solubilizing strain, MCR1.48, increased the shoot dry mass of A. polyphylla. This result indicates that phosphorous solubilization plays a key role in plant growth in trees.

9.4.4 The Agronomic Potential of Phosphate Solubilization by Endophytic Fungi from the Tropical Savanna Sustainable agriculture requires the use of strategies to increase or maintain the current rate of food production while reducing damage to the environment and human

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health. Because of the health effects of pollution related to chemical fertilizers and pesticides, interest in finding alternative green methods (Abo Nouh 2019). The use of microbial plant growth promoters is an alternative to conventional agricultural technologies. In this context, endophytes play an important role in growth promotion and resistance to various biotic and abiotic stresses and diseases in plants (Abo Nouh 2019; Azevedo and Quecine 2019). Similar to PGPR, these microorganisms have great potential to be used as safe and cost-effective alternatives to chemical fertilizers due to their wide range of plant growth-promoting activities (Abo Nouh 2019). The reduced availability of P in potentially productive acidic soils such as the Brazilian savanna requires plants to associate symbiotically with microorganisms, such as endophytes, that are adapted to those soil conditions (Zapata and Axmann 1995) and alter complexes that adsorb phosphate under acidic conditions, including FePO4 and AlPO4 (Andrade et al. 2003). The plant growth-promoting effects of endophytes include increased plant height and biomass of shoots, stems, and roots; lignification of the xylem vessels; and increased crop yield (Azevedo and Quecine 2019). In this context, phosphorus deficiency limits agricultural production, especially in acidic soils such as those of the Brazilian savanna (Nakayama et al. 1998). In this biome, the water-soluble P is transformed into iron phosphate (FePO4 ) and aluminum phosphate (AlPO4 ) (Silva et al. 2011), which are moderately soluble complexes (Son et al. 2006; Yadav et al. 2010; Chai et al. 2011). On the other hand, Vitorino et al. (2012) reported the capacity of endophytic fungi isolated from roots of Hyptis marrubioides Epling, a Brazilian savanna species, to solubilize calcium phosphate in GELP medium and iron phosphate in modified Reyes basal medium. Of six fungal strains analyzed by solubilization assays, none of the fungi tested solubilized CaHPO4 . In contrast, all of these fungi demonstrated the capacity to solubilize high levels of FePO4 . These authors suggested that none of the fungi strains tested solubilized CaHPO4 may be related to the fact that these fungi were isolated from the root system of H. marrubioides Epling, a plant adapted to acidic soil, in which P is bound to Fe3+ and to Al3+ (Khan et al. 2009). According to Sharma and Roy (2015), fungal endophytes were isolated from root, stem, and leaves of the plant Amaranthus spinosus, a species occurring in the savanna biome, stated that endophytic fungal isolates of the plant A. spiunosus showed a positive test for phosphate solubilization. The phosphate solubilization efficiency was found to be highest for the fungal genera Aspergillus isolated from the stem of the plant. In our research group, Torres (2018) studied 66 endophytic fungi isolated from Stryphnodendron adstringens and Solanum lycocarpum St. Hill collected in the Brazilian Tropical Savanna Reserve of the Federal University of São Carlos, Brazil. Healthy leaves and stems of both plants were collected and submitted to superficial asepsis. After incubation of the botanical material, isolation and molecular identification of the endophytic fungi were performed. The endophytic strains were evaluated in vitro for the solubilization of inorganic phosphate. These strains showed promise because of their ability to solubilize inorganic phosphate with mean phosphate solubilization indexes ranging from 1.46 to 1.93 and 1.19 to 2.61 for the strains isolated from S. adstringens and S. lycocarpum, respectively.

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9.5 Conclusion The search for interesting natural biological activities has been the basis for the development of various biotechnological and agricultural applications. The microbial world, and endophytes, in particular, exhibit vast genetic and metabolic biodiversity that has not yet been thoroughly explored. According to Azevedo and Quecine (2019), most studies on endophytes have been carried out using hosts from temperate countries, while data from tropical regions remain scarce. Available literature revealed that tropical plants host a great diversity of endophytic microorganisms, many of which are yet to be studied. The Phosphate-solubilizing endophytes are important not only because they contribute to plant growth but also because of their prospective commercialization to manufacture bio-fertilizers. An understanding of the ability and efficiency of microorganisms in solubilizing phosphates can allow the selection of lines with high potential for using them as biofertilizers. This application of microorganisms can replace or reduce the use of soluble phosphate fertilizers by better using the existing naturally or after amendments to the soil. Acknowledgements This work was supported by grants from the São Paulo Research Foundation, FAPESP (Proc. Nos. 2015/10974-8 and 2019/08867-0).

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Part III

Beneficial Microbes and Mineral Nutrient Management

Chapter 10

Endophytic Actinobacteria Associated with Mycorrhizal Spores and Their Benefits to Plant Growth Krisana Lasudee, Pharada Rangseekaew, and Wasu Pathom-aree

Abstract Actinobacteria are a large group of Gram-positive bacteria with a unique high G + C content(%) in their genome. They are best known as major producers of bioactive compounds in particular secondary metabolites. Arbuscular mycorrhiza or endomycorrhiza are the most common symbionts between plant roots and fungi with long historical practices in agriculture. Recently, it has become apparent that there are actinobacteria live in association with arbuscular mycorrhizal spores as “endophytes.” This special niche harbors diverse actinobacterial taxa with potential in the production of plant growth-promoting substances. The application of some of these actinobacteria exhibited growth enhancement in several plant species including those grown under abiotic and biotic stresses. Plant growth-promoting properties are common within members of actinobacteria occurring endophytically in mycorrhizal spores. A study of Streptomyces from Funneliformis mosseae spores to alleviate adverse effects of drought on Thai jasmine rice KDML105 is a neat evidence of its potential to promote plant growth sustainably. The diversity of endophytic actinobacteria from mycorrhizal spores and their possible application in agriculture as plant growth promoters are the main focus of this chapter. Keywords Actinobacteria · Mycorrhizal spores · Endophyte · Plant Growth-Promoting rhizobacteria · Drought

10.1 Introduction Actinobacteria are a large group of Gram-positive mostly filamentous bacteria with the characteristic of their high G+C content (%) in their DNA. Based on their genome K. Lasudee · P. Rangseekaew · W. Pathom-aree Microbiology Section, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand W. Pathom-aree (B) Research Center of Microbial Diversity and Sustainable Utilization, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_10

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analysis, the actinomycetes group of organisms is now renamed as actinobacteria. They are widely distributed in natural environments and established in cells and tissues of plants. Members of actinobacteria in particular Streptomyces spp. are major producers of antimicrobial agents and bioactive compounds, some of which are being used today as antibacterial, antifungal, anticancer, or cholesterol-lowering drugs (Barka et al. 2016). On the other hand, they have the potential to produce plant growth-promoting compounds and have biocontrol properties (Singh et al. 2018; Suarez-Moreno et al. 2019; Liotti et al. 2019). Actinobacteria can be used to improve plant growth and promote growth of plants under both abiotic and biotic stresses. Similar to other PGP bacteria, they can promote plant growth via direct and indirect mechanisms (Olanrewaju et al. 2017; Sathya et al. 2017; Vurukonda et al. 2018). Nitrogen fixation, phytohormones production, phosphate solubilization, siderophore production, etc., are considered as direct (Glick 2012; Hamadi and Mohammadipanah 2015; Vurukonda et al. 2018). Whereas indirect mechanisms include antibiotics production (Dinesh et al. 2017; Singh and Dubey 2018) and production of lytic enzymes to degrade the cell wall of fungal pathogens (Singh and Gaur 2016; Sathya et al. 2017; Gasmi et al. 2019). Thus, actinobacteria are attractive microorganisms with high potential for agricultural applications in terms of environmental sustainability and safety. The term mycorrhiza (from the Greek “mycos” meaning fungus and “rhiza” meaning root) was coined to describe the symbiotic association between plant root and fungi (Parniske 2008; Bonfante and Anca 2009). To date, at least 50,000 fungal species are suggested to form mycorrhizal associations with 250,000 plant species (van der Heijden et al. 2015). Arbuscular mycorrhiza (AM) is a type of endomycorrhiza in which the fungal hyphae penetrate host root cells. It is widespread in natural environments and can be found in more than 80% of living land plant species, liverworts, ferns, woody gymnosperms, angiosperms, and grasses (Bonfante and Anca 2009). Arbuscular mycorrhizal fungi (AMF) are obligate symbionts (Owen et al. 2015) and meant to improve the plant’s nutrient uptake and in turn plant provides AM fungi with carbon sources and habitat (Smith and Smith 2011). Several microbial taxa including members of both Gram-negative bacteria (Xavier and Germida 2003; Bharadwaj et al. 2008a, b; Battini et al. 2016; Lasudee et al. 2017) and Gram-positive bacteria including actinobacteria of the genus Streptomyces (Schrey et al. 2012; Mohandas et al. 2013; Poovarasan et al. 2013; Battini et al. 2016; Lasudee et al. 2018; Chaiya et al. 2019) associated with AM fungal spores have recently been reported. These mycorrhizal associated bacteria usually exhibited interesting biocontrol and plant growth-promoting activities (Mohandas et al. 2013; Poovarasan et al. 2013; Battini et al. 2016) thus make them attractive for application in sustainable agriculture. Drought stress induces damage to the biochemical and physiological processes of plants thus interfere with their normal functions (Pandey and Shukla 2015). Moreover, drought influences the nutrient availability and transportation in soil (GontiaMishra et al. 2016; Vurukonda et al. 2016). Currently, climate change is causing a reduction in precipitation and changed rainfall patterns. This changing climate leads

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to more frequent drought events that threaten crop productivity and global food security (Anjum et al. 2011; Fahad et al. 2017). Crop yields in more than 70% of global arable lands are affected by water deficits especially in Africa and Asia (Eke et al. 2019). About 85% of damage and loss in agriculture from 2010 to 2016 are related to drought with an estimated economical value of at least USD 29 billion (FAO 2018). For these reasons, drought is emerging as the most deleterious abiotic stress to crop production and yields worldwide. This chapter aims to summarize the current information on the diversity of actinobacteria associated with arbuscular mycorrhizal spores and their beneficial applications to promote plant growth. Special attention has been given to actinobacteria associated with Funneliformis mosseae spores and their ability to promote rice growth under drought conditions.

10.2 Endophytic Actinobacteria from Mycorrhiza Mycorrhizal fungi interact with several actinobacteria in all stages of their life cycle (Frey-Klett et al. 2007). This associated actinobacterial population has a versatile role in health promotion in positive ways by way of root colonization, stimulate hyphal, and spore germination of their mycorrhizal host (Roesti et al. 2005). In turn, mycorrhizal fungi support the growth of associated bacteria by providing habitat and nutrients. However, the exact role of these associated bacteria is yet to be established. Endophytic bacteria adhere to the arbuscular mycorrhiza hyphae (Bianciotto et al. 1996; Manfeld-Giese et al. 2002) and or embeded within the outer AM spore wall layer (Walley and Germida 1996) or penetrate inner layer of spore (Roesti et al. 2005). Actinobacteria frequently found inside the mycorrhizal spores. Mycorrhizal spore-associated actinobacteria have been isolated, characterized, and applied to the plants for their growth as summarized in Table 10.1. Most of the actinobacteria isolated from mycorrhizal spores are filamentous including species of Amycolatopsis, Intrasporangium, Nocardioides, Pseudonocardia, Streptomyces, Streptoverticillium, etc. From all filamentous genera, Streptomyces spp. remained the most abundant actinobacteria found from several mycorrhizae for example Glomus mosseae (Mohandas et al. 2013), Rhizophagus intraradices (Battini et al. 2016), and F. mosseae (Lasudee et al. 2018). Other nonfilamentous actinobacteria including Arthrobacter, Cellulomonas, Corynebacterium, Curtobacterium, Leifsonia, Mycobacterium, Nocardia, Propionibacterium, and Streptosporangium (Bharadwaj et al. 2008b; Poovarasan et al. 2013; Battini et al. 2016; Long et al. 2017) were also found invarious genera of mycorrhizal spores. The standard isolation methods for actinobacteria occurring inside mycorrhizal spores generally involve 3 steps (i) surface sterilization of mycorrhizal spores, (ii) destruction of the spore cell wall, and (iii) cultivation of actinobacteria on selective media. For surface sterilization, different chemicals were used including 2% Clorox (Lee and Koske 1994), chloramine (Mohandas et al. 2013), 4% (w/v) chloramine T trihydrate (Chaiya et al. 2019), 2% sodium hypochlorite, and 70% (v/v) ethanol

Taxa

Nocardia sp. Streptomyces sp.

Streptomyces spp. Nocardia spp. Streptosporangium Streptoverticillium Intrasporangium Norcardiodes

Arthrobacter spp. Micrococcus spp. Cellulomonas flavigena Aureobacterium saperdae Clavibacter michiganense subsp. nsidiosum Curtobacterium citreum Corynebacterium bovis

Streptomyces fradiae Streptomyces avermitilis Streptomyces cinnamonenesis Streptomyces canus Leifsonia poae Streptomyces netropis Streptomyces scabies Streptomyces griseus Streptomyces violarus Streptomyces albidoflavus

Mycorrhiza

Gigaspora gigantia

Glomus macrocarpum

Glomus mosseae or Glomus intraradices

Glomus mosseae

Table 10.1 Actinobacteria from mycorrhizal spores and isolation media

Rhizophere of guava (Psidium guajava L. cv Arka Mridula), Karnataka State, southern India

Rhizopheres soils of Festuca ovina or Leucanthemum vulgare

Soils from the edge of a non-irrigated barley field in Yolo Country, California, USA

Barrier sand dune at Moonstone Beach, Rhode Island (RI)

Source of AM spore

Ames et al. (1989)

Lee and Koske (1994)

References

Ken Knight agar, incubated at 28 °C ± 2 for 2–7 days

(continued)

Poovarasan et al. (2015)

Mohandas et al. (2013); Poovarasan et al. (2013); Poovarasan et al. (2015)

Tryptic soy broth agar at Bharadwaj et al. 25 °C in the dark for 48 h (2008b)

Solidified chitin water agar at 25–27 °C for 4 weeks

MYPT agar at room temperature (21–27 °C) for up to two weeks

Media

232 K. Lasudee et al.

• Curtobacterium luteum M060824-7 the Ministry of • Mycobacterium mucogenicum M060824-8 Agriculture, Forestry, and • Streptomyces sp. Fisheries Gene bank, Tsukuba, Japan

• • • • • •

Amycolatopsis eburnea sp. nov

Gigaspora margarita MAFF 520054 spores

Funneliformis mosseae CMU-RYA08

Funneliformis mosseae RYA08

Agarwood (Aquilaria crassna Pierre ex Lec.) rhizophere soil,Klaeng, Rayong province, Thailand

Pseudonocardia nantongensis isolate SP Soil of a Aquilaria crassna Streptomyces thermocarboxydus isolate 48 plantation in Rayong Streptomyces spinoverrucosus isolate S1 Province, Thailand Streptomyces thermocarboxydus isolate S3 Streptomyces pilosus isolate S4 Streptomyces pilosus isolate S4-1

Pot-culture maintained in the collection of Microbiology Labs of the Department of Agriculture, Food and Environment, University of Pisa, Italy

Streptomyces spp. Arthrobacter phenanthrenivorans Nocardiodes albus

Rhizophagus intraradices isolate IMA6

Source of AM spore

Taxa

Mycorrhiza

Table 10.1 (continued) References

Lasudee et al. (2018)

Long et al. (2017)

Actinomycetes isolation Chaiya et al. (2019) agar at 30 °C for a month

Starch casein agar and humic acid vitamin agar at 30 for up to 4 week

Tryptic Soy Agar (TSA) at 26 °C for 7 days

Waksman’s agar at 28 °C Battini et al. (2016) for 7 days

Media

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(Lasudee et al. 2018). The treatment time given for each chemical is varied depending on the concentration for example, Glomus mosseae spores were decontaminated with chloramine-T for 30 min (Mohandas et al. 2013). Alternatively, F. mosseae CMURYA08 spores were surface sterilized by 2% sodium hypochlorite for 1 min followed by 70% (v/v) ethanol (Lasudee et al. 2018) or by 4% (w/v) chloramine T trihydrate for 10 min (Chaiya et al. 2019). The spore cell wall could be broken by simple grinding with a sterile micro pestle. However, the suspending solution varied depending on author preferences. These solutions are steriled distilled water, phosphate buffer saline (PBS), and 0.75% sodium chloride. Several selective media have been used for isolation of endophytic actinobacteria from mycorrhizal spore namely ken knight agar (Poovarasan et al. 2015), Waksman’s agar (Battini et al. 2016), starch casein agar, humic acid vitamin agar (Lasudee et al. 2018), actinomycetes isolation agar (Chaiya et al. 2019), etc. Furthermore, a general cultivation medium such as tryptic soy agar (TSA) was also used for isolation (Long et al. 2017). Special media such as solidified chitin water agar was reported for isolation of chitinase producing actinobacteria from calcareous soil (Ames et al. 1989). Moreover, the enrichment procedure proved successful for the isolation of endophytic actinobacteria from F. mosseae spores. Lasudee et al. (2018) soaked the spores in soil extract broth and shaken at 120 rpm at room temperature for 1 h to enrich endophytic actinobacteria. This procedure was considered to be essential because the isolation of actinobacteria without an enrichment step led to the possibility of not getting actinobacterial growth on selective media.

10.3 Plant Growth-Promoting (PGP) Activities of Endophytic Actinobacteria Mycorrhiza is the association of a fungus and root plants (Mohandas et al. 2013) that play an important role in the agriculture ecosystem. The colonization of mycorrhizal fungi in root helps to promote plant growth via nutrient mobilization, biocontrol activity, etc. Interestingly, there are reports considering actinobacteria that can promote plant growth by different mechanisms both directly and indirectly.

10.3.1 Endophytic Actinobacteria Associated with Nutrient Uptake in Plants Endophytic actinobacteria promote plant growth directly by facilitating the nutrient acquisition of plants via many mechanisms including siderophore production and solubilization of phosphate, phytate, or zinc as summarized in Table 10.2. Phosphorus (P) is an essential macronutrient for the growth and development of plants (Behera et al. 2014). However, most phosphorus in the soil is available

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Table 10.2 Bioactivities related to nutrient uptake of endophytic actinobacteria from mycorrhizal spores Mycorrhiza

Taxa

Bioactivities

Glomus mosseae

Streptomyces avermitilis Streptomyces canus Leifsonia poae

• Production Mohandas of et al. siderophore (2013); Poovarasan et al. (2013); Poovarasan et al. (2015)

Streptomyces avermitilis Streptomyces canus Leifsonia poae Streptomyces fradiae Streptomyces netropis Streptomyces scabies Streptomyces griseus Streptomyces violarus Streptomyces albidoflavus Streptomyces cinnamonenesis

• Phosphate and zinc solubilization • Organic acid production (such as gluconic acid)

Streptomyces spp. Nocardiodes albus

• Phosphate Battini and phytate et al. (2016) solubilization

Arthrobacter phenanthrenivorans

• Siderophore production

Rhizophagus intraradices isolate IMA6

Funneliformis Pseudonocardia sp. isolate SP mosseae CMU-RYA08 • Streptomyces pilosus isolate S4 • Streptomyces pilosus isolate S4-1 • Streptomyces thermocarboxydus isolate 48 • Streptomyces spinoverrucosus isolate S1 • Streptomyces thermocarboxydus isolate S3

References

• Siderophore Lasudee production et al. (2018)

• Siderophore production • Phosphate solubilization

in insoluble forms which plants cannot uptake (Glick 2012). In soils, phosphorus usually exists in two forms insoluble inorganic and insoluble organic forms. Phosphorus can be bound with hydrated oxides such as aluminum (Al), iron (Fe), and manganese (Mn) that are poorly dissolved and assimilated (Behera et al. 2014). Similar to bacteria in soil, actinobacteria solubilize phosphate via mechanism: (i) production of organic acids (ii) secretion of enzymes. Some actinobacteria synthesize organic acids to solubilize inorganic phosphorus. Actinobacteria isolated from G. mosseae were able to solubilize tricalcium phosphate and aluminum phosphate by producing at least four organic acids (Poovarasan et al. 2015). In general, these

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actinobacteria produced gluconic acid as the major organic acid for phosphate solubilization (Mohandas et al. 2013; Poovarasan et al. 2015). Similarly, S. thermocarboxydus isolates S3 from F. mosseae CMU-RYA08 produced gluconic acid, malonic acid, oxalic acid, and propionic acid to solubilize tricalcium phosphate (Lasudee et al. 2018). Also, Streptomyces spp. and Arthrobacter phenanthrenivorans isolated from Rhizophagus intraradices were able to solubilize both insoluble organic (inositol phosphate) and insoluble inorganic phosphates (tri-calcium phosphate). Phosphate solubilizing ability was reported as solubilization efficiency (SE) (Battini et al. 2016). Also, zinc solubilization was reported in some Streptomyces species isolated from G. mosseae (Poovarasan et al. 2015). Iron is an important micronutrient for the growth of both plants and bacteria. Although iron is abundant in soils, it exists in the form of ferric iron which is insoluble. Thus, the amount of iron available to plants and bacteria is low (Glick 2012; Sathya et al. 2017). Siderophores are ferric iron (Fe3+ ) specific chelators that can promote plant growth both by direct and indirect mechanisms. Under limiting iron environment, actinobacteria secrete siderophores directly to bind with ferric iron before uptake. Siderophores also act as a biocontrol agent for indirect mechanisms. With a higher affinity for iron than fungal pathogens, siderophores from biocontrol actinobacteria outcompete pathogens causing insufficient iron necessary for phytopathogen proliferation (Glick 2012). Siderophores have been detected from Streptomyces species isolated from mycorrhiza by observing yellow-orange halo around the colony. Unfortunately, the determination of siderophore types was not investigated in the paper published (Mohandas et al. 2013; Battini et al. 2016). The only report by Lasudee et al. (2018) determined the type of siderophore produced by actinobacteria isolated from F. mosseae spores and it comes out as hydroxamate and catecholate type siderophores.

10.3.2 Biocontrol Activities of Endophytic Actinobacteria Actinobacteria can also promote plant growth via indirect mechanisms as biocontrol agents as summarized in Table 10.3. Several actinobacteria associated with mycorrhizal spores have been reported to suppress the growth of plant pathogens (Bharadwaj et al. 2008b; Mohandas et al. 2013; Poovarasan et al. 2013). For example, Streptomyces and Leifsonia species isolated from G. mosseae inhibited Fusarium oxysporum (guava wilt) and Alternaria solani (early blight of tomato) up to 96.4– 98.8% that is possible by the production of chitinase to degrade fungal cell wall. (Mohandas et al. 2013). Other hydrolytic enzymes such as amylase, cellulase, lipase, and protease were also reported from Streptomyces spp. and L. poae from G. mosseae (Poovarasan et al. 2015). Later, the similar set of actinobacteria was found to inhibit Xanthomonas axonopodis pv punicae (bacterial blight disease) as studied by (Poovarasan et al. 2013). Actinobacteria isolated from G. moseae or G. intraradices such as Arthrobacter spp., Micrococcus spp., and Cellulomonas flavigena exhibited antagonistic activity against Rhizoctonia solani (damping-off, cutting

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Table 10.3 Biocontrol activities of endophytic actinobacteria from mycorrhizal spores Mycorrhiza

Taxa

Biocontrol activities

Glomus macrocarpum

Streptomyces spp. Nocardia spp.

• Chitinase activity Ames et al. (1989) • Antimicrobial activity

References

Streptosporangium Streptoverticillium Intrasporangium Norcardiodes

• Chitinase activity

Glomus mosseae or Glomus intraradices

Arthrobacter spp. Micrococcus spp. Cellulomonas flavigena

Inhibition of Rhizoctonia solani

Bharadwaj et al. (2008b)

Glomus mosseae

Streptomyces fradiae Streptomyces avermitilis Streptomyces cinnamonenesis Streptomyces canus Leifsonia poae

• Chitinase activity • Hydrolytic enzymes (chitinase, cellulose, amylase, protease, and lipase) • Antifungal activity (Fusarium oxysporum and Alternaria solani) • Antibacterial activity against Xanthomonas axonopodis pv punicae

Mohandas et al. (2013); Poovarasan et al. (2013); Poovarasan et al. (2015)

Streptomyces netropis Streptomyces scabies Streptomyces griseus Streptomyces violarus Streptomyces albidoflavus

• Chitinase activity • Hydrolytic enzymes (chitinase, cellulose, amylase, protease, and lipase)ara>

Poovarasan et al. (2015)

decay, stem girdling, and aerial blight). The potential antagonistic isolates were identified as Arthrobacter oxydans, Cellulomonas flavigena, and Micrococcus kristinae (Bharadwaj et al. 2008b). Earlier, Streptomyces spp. and Nocardia sp. isolated from G. macrocarpum showed antibacterial activity against 11 tested bacteria including rhizobia and fluorescent Pseudomonas sp. and six fungi (Ames et al. 1989).

10.3.3 Phytohormone Production by Endophytic Actinobacteria Actinobacteria from mycorrhizal spores can produce phytohormones as summarized in Table 10.4. In vitro, actinobacteria produced IAA in tryptophan supplemented culture broth for the synthesis of IAA (Spaepan and Vanderleyden 2011). Streptomyces species produced IAA at a varying quantity of 4.44–11.12 µg/ml. S. thermocarboxydus isolate S3 isolated from F. mosseae CMU-RYA08 produced the

• Streptomyces thermocarboxydus isolate S3 IAA

IAA

• • • •

Funneliformis mosseae CMU-RYA08

Streptomyces thermocarboxydus isolate 48 Streptomyces spinoverrucosus isolate S1 Streptomyces pilosus isolate S4 Streptomyces pilosus isolate S4-1

• Curtobacterium luteum isolate M060824-7 ND • Mycobacterium mucogenicum M060824-8

Gigaspora margarita MAFF 520054 spores

IAA

Streptomyces spp.

IAA

Streptomyces avermitilis

Rhizophagus intraradices isolate IMA6

IAA and gibberellin

Streptomyces fradiae Streptomyces cinnamonenesis Streptomyces canus Leifsonia poae

Glomus mosseae

Hormone production

Taxa

Mycorrhiza

Table 10.4 Plant growth-promoting activities of endophytic actinobacteria from mycorrhizal spores

• Promotion of mung beans (Vigna radiata) growth • Promotion of rice (Oryza sativa) growth in low nutritional soil under induced drought stress

ND

• Promotion of alfafa (Medicago sativa) growth

ND

• Promotion of growth of guava (Psidium guajava L.) • Promotion of pomegranate (Punica granatum L.cv Bhagwa) growth

• Promotion of growth of guava (Psidium guajava L.) • Promotion of pomegranate (Punica granatum L.cv Bhagwa) growth

Plant growth-promoting activities

Lasudee et al. (2018)

Long et al. (2017)

Battini et al. (2016)

Mohandas et al. (2013); Poovarasan et al. (2013); Poovarasan et al. (2015)

References

238 K. Lasudee et al.

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maximum IAA of 11.12 µg/ml (Lasudee et al. 2018). In addition, Leifsonia poae associated with Glomus mosseae produced IAA at 8.3 µg/ml (Mohandas et al. 2013). Similarly, Gibberellin (GA) is another plant hormone stimulating stem elongation, bolting, and flowering (Hamadi and Mohammadipanah 2015). Various species such as S. fradiae, S. cinnamonenesis, S. canus, and L. poae isolated from Glomus mosseae were reported to produce gibberellin in culture broth with the maximum GA of 12 µg/ml. reported by S. canus (Mohandas et al. 2013).

10.4 Beneficial Effects of Endophytic Actinobacteria on Plant Actinobacteria can promote plant growth by their ability to produce plant growth regulators. Several endophytic actinobacteria were reported to produce plant growth regulators such as IAA or siderophores in vitro as a result of these can promote plant growth under controlled environmental conditions (El-Tarabily et al. 2009; Mohandas et al. 2013). Mohandas et al. 2013 tested five actinobacteria associated with G. mosseae namely S. fradiae, S. avermitilis, S. cinnamonensis, S. canus, and L. poae for growth promotion of guava (Psidium guajava L.). Except for S. fradiae all of them increased height, leaf area, fresh weight, and dry weight of 10 months guava seedlings. Also, these actinobacteria promoted the growth of pomegranate, increased shoot and root length, leaf area, and total biomass in 6-month-old seedlings (Poovarasan et al. 2013). S. canus, increased dry weight over control possibly by its ability to produce growth hormones IAA and GA3 in vitro. Endophytic actinobacteria from Gigaspora margarita spores have recently been reported to promote the growth of alfalfa (Medicago sativa) seedlings. Similarly, Curtobacterium luteum M0608247 and Mycobacterium mucogenicum M060824-8 enhanced fresh and dry weight of leaf/stem and root fresh weight of alfalfa seedlings. Besides, these two actinobacteria also increased AMF colonization in alfalfa root (Long et al. 2017). Funneliformis belongs to a member of AMF in the family Glomeraceae, which form symbiotic relationships with many angiosperm plant roots. It was formerly known as Glomus mosseae until the genus Funneliformis was established in the year 2010 with F. mosseae as a type species (Schubler and Walker 2010). Being its wide occurrence and richness of literature, F. mosseae widely used as bioinoculant (Kruger et al. 2012). Its symbiosis with host plants improves the nutrient uptake and provides AM fungi with carbon sources (Rouphael et al. 2015; Wang et al. 2017; Begum et al. 2019). In the authors’ laboratory, S. thermocarboxydus spp have been isolated from F. mosseae spores (Fig. 10.1). The isolate S3 exhibited as plant growth-promoting bacteria due to its ability to produce IAA, ACC deaminase, and siderophore and solubilize insoluble phosphate. Interestingly, this species grew at a low water activity (aw 0.919) and was able to produce IAA under such conditions in vitro (Lasudee et al. 2018). Mung bean (Vigna radiata) inoculated with S. thermocarboxydus isolate S3

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Fig. 10.1 Spores of arbuscular mycorrhiza, Funneliformis mosseae; a under stereo microscope, b under light microscope (100x)

showed an increase in fresh weight, root and shoot length. Intense roots were also observed in both treatments. These results suggested that the beneficial effects on mung bean were responsible due to IAA production by S. thermocarboxydus isolate S3. IAA is known for its effect on the production of lateral roots and the promotion of root length (Etesami et al. 2015). Interestingly, under drought and low nutrient soil, S. thermocarboxydus isolate S3 can promote the growth of Thai jasmine rice (Oryza sativa) KDML105. This world-famous rice variety is sensitive to drought (Cha-um et al. 2010). After 46 d S. thermocarboxydus isolate S3 mitigated adverse effects of rice plants under induced drought conditions as observed in enhancement of the root, stem, total length, and dry weight which were higher than control plants (Fig. 10.2). Besides, S. thermocarboxydus isolate S3 benefited the physiological conditions of the rice plants as exemplified by increased in total chlorophyll and proline contents. Proline accumulation was proposed as one of the mechanism of drought tolerance in rice (Pandey and Shukla 2015). S. thermocarboxydus isolate S3 also maintain high relative water content (RWC) in inoculated leaves under drought conditions as shown in Fig. 10.3. The rice plants in the control treatment were withered and did not survive, whereas, in the treatment with S. thermocarboxydus isolate S3, some plants were still green at the end of the experiment. These positive effects on Thai jasmine rice (Oryza sativa) KDML105 are likely the effect of inoculation of S. thermocarboxydus isolate S3 which showed long-term effect as this isolate was re-isolated from rice roots (Lasudee et al. 2018). This finding suggested that S. thermocarboxydus isolate S3 could survive and live within the root tissues of rice. The beneficial effects of S. thermocarboxydus isolate S3 inoculation suggested to be a result of its PGP properties, in particular ACC deaminase activity and IAA production. Mycelium of S. thermocarboxydus isolate S3 was also observed on rice root as shown in Fig. 10.4. The observation of these typical filamentous cells of Streptomyces on the root surface and detection of S. thermocarboxydus isolate S3 from the root tissues strongly

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Fig. 10.2 Growth promotion of Thai jasmine rice (O. sativa) KDML105 by S. thermocarboxydus isolate S3 under drought conditions. a root, stem and total length; b dry weight, chlorophyll content; c proline content

Fig. 10.3 Thai jasmine rice (O. sativa) KDML105 inoculated with S. thermocarboxydus isolate S3 under drought. 1a isolate S3; 2a control; b root of inoculated rice; c root of uninoculated rice

indicated that this isolate was able to colonize rice roots. Similar results of bacterial colonization in rice roots have been reported (Etesami et al. 2014; Qin et al. 2017). This root colonization is an important factor in both plant growth-promoting activities and the survival of bacteria under drought conditions(Gontia-Mishra et al. 2016).

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Fig. 10.4 Photomicrograph of S. thermocarboxydus isolate S3 colonization surface of Thai jasmine rice (O. sativa) KDML105 under light compound microscope (100x)

10.5 Conclusions Based on the data from previous literature and our laboratory, it is evident that endophytic actinobacteria exist inside several species of arbuscular mycorrhizal spores. Several cultivable taxa have been isolated comprising Streptomyces as the most dominant genus. These actinobacteria exhibit plant growth-promoting properties in vitro and planta. S. thermocarboxydus isolate S3 was successfully isolated as an endophyte of F. mosseae spores. This endophytic Streptomyces showed potential to support the growth of Thai jasmine rice KDML105 under drought by improving nutrient uptake possibly through the production of IAA, siderophores, and phosphate solubilization. Other Streptomyces also efficiently suppressed the growth of important plant pathogens. The ability of actinobacteria from mycorrhizal spores to control plant pathogens and produce plant growth-promoting agents supports the possibility of using these actinobacteria for sustainable agriculture. The potential of non-filamentous or rare actinobacteria is yet to be explored to their full potential. The development of new or improved isolation methods is in urgent need to tap into the complete diversity of endophytic actinobacteria within mycorrhizal spores. Thus the role of these endophytic actinobacteria on their mycorrhizal host remains to be clarified which merits future investigation.

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Chapter 11

Endophytes as Plant Nutrient Uptake-Promoter in Plants Carlos García-Latorre, Sara Rodrigo, and Oscar Santamaría

Abstract Endophytic fungi, while living asymptomatically within plants, may confer competitive advantages such as resistance against biotic and abiotic stresses. Among them, the improvement in plant nutrient uptake is a phenomenon that has been explored for its potential use in agriculture, especially considering the need for a more sustainable farming model that integrates soil regeneration cycle and mitigation of the climate change effects. The utilization of fungal endophytes may enhance the absorption of macro and micronutrients for a wide diversity of plant species, which may reduce the application of chemical fertilizers. The processes involved in this higher nutrient uptake range from (i) the production of phytochemicals-like substances that favor root growth and increase mass flow or root interception of nutrients, (ii) by production of siderophores that bind Fe3+ , (iii) performing beneficial interaction with other soil organisms (iv) the interception of nutrients via hyphae, and (v) due to the secretion of substances such as hydrolytic enzymes that increase nutrient solubilization. These effects may counter multiple benefits to plants growing under stressful conditions. The main role of endophytes in mineral nutrient uptake in plants has been elucidated. Keywords Fungal endophytes · Nutrient uptake · Biotic and abiotic stress

11.1 Introduction Fungal endophytes are an important group of plant microbes living asymptomatically and sometimes systemically within plant tissues (Carroll 1991; Hardoim

C. García-Latorre · S. Rodrigo School of Agricultural Engineering. Institute of Dehesa Research, University of Extremadura, Avda., Adolfo Suárez s/n 06007 Badajoz, Spain O. Santamaría (B) Department of Construction and Agronomy, University of Salamanca, Avenida Cardenal Cisneros 34, 49029 Zamora, Spain e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_11

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et al. 2015). Initially, it was presumed that endophytic fungi only colonized aboveground plant tissues (leaves, stems, bark, petioles, and reproductive structures), which distinguished them from mycorrhizal fungi. Later, numerous studies nowadays have demonstrated that fungal endophytes may also inhabit root tissues (Huang et al. 2019; Li et al. 2019; Strom et al. 2019; Yamaji et al. 2016). Overall, endophytic fungi are ubiquitous and extremely diverse in host plants; in fact, every plant examined with this purpose has been found to harbor at least one species of endophytic fungus (Arnold et al. 2000; Saikkonen et al. 2000). Furthermore, it is interesting to note that such a high diversity, i.e. more than 100 different species can be found in a single plant species (Sánchez et al. 2012). Researches on fungal endophytes have increased in recent years and an increasing number of studies exhibited the beneficial effects of diverse endophyte species on their plant hosts. Several endophytes have been shown to confer resistance to plants against herbivores and phytopathogens (Clay and Schardl, 2002; Rodrigo et al. 2017; Romeralo et al. 2015), to improve the nutritional status of the plant host (Lledó et al. 2016), and its competitiveness toward other plant species (Vázquez de Aldana et al. 2013), to increase its photosynthetic efficiency (Spiering et al. 2006), antioxidant capacity (Hamilton and Bauerle 2012) and increase plant adaptation to stressful habitats such as of drought (Giauque and Hawkes 2013), salinity (Redman et al. 2011), and heavy metals (Zamani et al. 2015). These studies provide pieces of evidence regarding the important role played by endophytes in the adaptation and survival of plants even under stressful habitats and conditions. The endophytes have been identified as an important source of novel and diverse active secondary metabolites of great scientific and industrial interest (Brader et al. 2014; Dheeman et al. 2017; Schulz et al. 2002; Surup et al. 2018). These active metabolites, often involved in the beneficial effects observed in plant hosts, might confer their adaptation capacity toward stressful conditions, and their resistance in adverse field conditions. For instance, metabolites produced by Penicillium citrinum Thom isolated from Ixeris repens (L.) A.Gray, when applied in Carex kobomugi Ohwi showed better growth, higher chlorophyll and carotenoids content, as well as higher efficiency in carboxylation and the water use (Hwang et al. 2011).

11.2 Enhancing Plant Nutrient Uptake In the last decades of the twentieth century, the importance of soil as a basic environmental component has been highlighted, recognizing that soil is a nonrenewable resource that virtually needs time for its regeneration or nutrients replacement (Nortcliff 2002). Sustainable soil management practices are essential for maintaining proper soil health for the future production of crops. However, the intensification of the cropping systems, which is causing salinization in many soils especially in arid and semi-arid regions (Khan et al. 2005), and climate change (reducing the amount of available water for crops) are contributing to the soil quality deterioration and decreasing the availability of the nutrients for plants. Under this scenario, the

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design of agricultural systems that aims to reduce inputs of chemicals and using the endophyte microbes to maximize the efficiency of such resources might be of great importance (Maheshwari 2017; Tilman et al. 2002). Thus, the endophytic fungi that enhance the nutrient uptake by their plant hosts (Lledó et al. 2015) could play an important role in more sustainable agriculture systems. This may allow reducing the number of chemical fertilizers for enhancing plant growth, and consequently productivity (Silveira and Kohmann 2020), or by improving food or feed nutritional quality by increasing the concentration of some minerals in the edible parts, especially when considering the requirement of some essential minerals for animals and humans, such as I, Fe, Zn, and Se, that usually present deficiency (Graham et al. 2007; White and Broadley 2005). As supporting knowledge for the eventual use of endophytes with that purpose, several studies have reported the enhancement of the nutrient uptake in plants caused by endophytes, as summarized in Table 11.1. The endophyte Epichloë festucae Leuchtm., Schardl and Siegel has been found to increase the uptake of P, N, Zn, Ca, or Mg by Festuca rubra L. plants (Vázquez de Aldana et al. 2013; Zabalgogeazcoa et al. 2006) and accumulation of Mn by Lolium perenne L. in its herbage (Soto-Barajas et al. 2016). Other endophytes belonging to Neotyphodium genus have been reported in increasing the concentration of Zn and Mo in L. perenne (Malinowski et al. 2004) and the concentration of P, Ca, or Zn in Festuca arundinacea Schreb. (Malinowski et al. 2000). According to Lledó et al. (2015), when the endophyte Stemphylium globuliferum (Vestergr.) Simmons was inoculated in Poa pratensis L., its herbage showed higher values in the concentration of Ca (from 0.78 to 0.90 mg/kg), Mg (from 0.31 to 0.36 mg/kg), and Sr (from 68.07 to 77.68 mg/kg) in comparison to that of uninoculated plants. Authors reported a significant increase in the Al, B, Fe, Li, Mo, Ni, and Ti uptake when plants were inoculated with Epicoccum nigrum Link, while the inoculation of Fusarium lateritium Nees in P. pratensis caused an increase in the concentration of Fe, Ni, and Zn in the herbage by 31%, 32%, and 16%, respectively, in comparison with the uninoculated controls. An increase in the Fe uptake by endophyte-infected plants has also been reported by Bartholdy et al. (2001), and Johnson et al. (2013), when studied the influence of Phialocephala fortinii Wang and Wilcox, and Epichloë/Neotyphodium on forest tree species and Lolium perenne, respectively. Also, Phomopsis liquidambari Chang, Jiang, and Chi, a mutualistic rice symbiont, promoted rice growth and grain yield at the same time that significantly reduced the amount of soil N fertilizer required for optimum plant growth (Li et al. 2009; Yuan et al. 2007). Although most of the studies have been focused on grass species hosts, the positive influence of endophytes on the uptake and later accumulation of minerals has also been reported in other host families, such as legumes. Thus, in Ornithopus compressus L. plants, the endophytes Stemphylium sp., Fusarium sp., Sordaria fimicola (Roberge ex Desm.) Ces. and De Not., and Sporormiella intermedia (Auersw.) Ahmed and Cain ex Kobayasi were found to cause a higher accumulation of B, Mo, P, S and Zn in the herbage than in controls (endophyte-free plants) in a study conducted by Santamaria et al. (2017). Likewise, Stemphylium globuliferum caused a higher accumulation of Ca, Cd, Cu, Mn, Pb and Zn (more than 31, 217, 66, 14, 305 and

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Table 11.1 Summary of the effects on the nutrient uptake produced by endophytic fungi on different plant species Endophyte species

Plant host

Functional effect (nutrient uptake increase)

Reference

Phialocephala fortinii

Pinus contorta Douglas

N, P

Jumpponen et al. (1998)

Trichoderma sp.

Cucumis sativus L.; Fe, Zn, Cu, Mn, Solanum lycopersicum (influence on AM L. fungi)

Yedidia et al. (1999); Nzanza et al. (2012)

Neotyphodium sp.

Festuca arundinacea Schreb

P, Ca, or Zn

Malinowski et al. (2000)

Phialocephala fortinii

In vitro

Fe (siderophores)

Bartholdy et al. (2001)

Neotyphodium sp.

Lolium perenne L.

Zn, Mo

Malinowski et al. (2004)

Epichloë festucae

Festuca rubra L.

P, N, Zn, Ca, Mg

Zabalgogeazcoa et al. (2006); Vázquez de Aldana et al. (2013)

Phomopsis liquidambari

Oryza sativa L.

N Rice growth promoter

Yuan et al. (2007); Li et al. (2009)

Order Helotiales

Deschampsia Antarctica Desvaux

N

Upson et al. (2009)

Epichloë festucae

Lolium perenne L.

Fe

Johnson et al. (2013)

Stemphylium globuliferum

Poa pratensis L.

Ca, Mg, Sr

Lledó et al. (2015)

Epiccocum nigrum

Poa pratensis L.

Al, B, Fe, Li, Mo, Ni, Ti

Fusarium lateritium

Poa pratensis L.

Fe, Ni, Zn

Trichoderma atroviridae and AM 1 fungi (Glomus sp.)

Triticum durum Wesf

Grain Protein, P, K, Fe Leaf N, P, K, Fe, Zn

Colla et al. (2015)

Stemphylium globuliferum

Trifolium subterraneum L.

Ca, Cd, Cu, Mn, Pb, Zn

Lledó et al. (2016)

Order Pleosporales

Trifolium subterraneum L.

K, Pb

Epichloë festucae

Lolium perenne L.

Mn

Soto-Barajas et al. (2016)

Stemphylium sp.

Ornithopus compressus L.

B, Mo, P, S

Santamaría et al. (2017)

Fusarium sp.

Ornithopus compressus L.

B, Mo, P, S, Zn (continued)

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Table 11.1 (continued) Endophyte species

Plant host

Functional effect (nutrient uptake increase)

Sordaria fimicola

Ornithopus compressus L.

B, Mn, Mo, S, Zn

Sporormiella intermedia

Ornithopus compressus L.

B, Mn, Mo, P, S, Zn

DSE 2 endophytes

Solanum lycopersicum N, P, K, Ca, Mg, L. Fe, Mn, Zn

1 AM:

Reference

Vergara et al. (2017)

Arbuscular mycorrhizal fungi; 2 DSE: Dark septate endophyte

60%, respectively in comparison with free-endophyte plants) when it was inoculated in Trifolium subterraneum L. plants cultivated under greenhouse conditions (Lledó et al. 2016). Such effects were dependent on environmental conditions, because when the same endophytic species was inoculated in the parent host T. subterraneum, under field conditions, the increase in the concentration of minerals was recorded in Al, Fe, Pb, and Li (Lledó et al. 2016). In a similar study, in the experiments performed in the field, an endophyte belonging to Pleosporales order named as E244, was found to increase concentration of K (72%) and Pb (225%) when compared to the control (uninfected plants) which inoculated in the aerial tissues of the plant host. On the other hand, the enhancement of nutrient uptake in plants caused by fungal endophytes is mainly achieved indirectly. In the case of Trichoderma spp. in addition to their biocontrol activity, this endophyte can improve the solubility of soil micronutrients such as Fe, Zn, Cu, and Mn, due to its influence on arbuscular mycorrhiza (AM) activity (Yedidia et al. 1999; Nzanza et al. 2012). Thus, in order to understand it more, wheat seeds coated with an AM fungus and Trichoderma atroviride Karst., once cultivated in the field, produced grain with a higher nutritive value in terms of protein, P, K, and Fe (Colla et al. 2015). According to authors, it was probably due to the higher chlorophyll content and the higher photochemical activity of the pigment-protein complex, photosystem II (PSII), besides better nutritional status (higher leaf content of N, P, K, Fe, and Zn) of the wheat plant. On the other hand, a specific group of endophytes named as dark septate endophytes (DSE) has also been observed to cause an enhancement of the mineral uptake in pine seedlings (Jumpponen et al. 1998), by increasing their uptake of P and N in presence of DSE, and in Deschampsia antarctica Desvaux plants inoculated with DSE, which increased their N uptake (Upson et al. 2009). Furthermore, Vergara et al. (2017) reported the potential of DSE fungi to promote the uptake of macro and micronutrients more efficiently, resulting in increased tomato plant growth.

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11.3 Endophytes Mediated Mechanisms of Action to Enhance Nutrients Uptake Several mechanisms have been proposed to be involved in the enhancement of the mineral uptake by host plant as a consequence of the endophyte infection (Fig. 11.1). The production of substances with plant growth promoting (PGP) properties, such as phytohormone-like substances (i.e. auxins, gibberellins, etc.) and phytochemicals has highly beneficial effects on the growth enhancement of the host plant (Khan et al. 2016). Earlier, Assuero et al. (2006) reported enhancement of root growth which resulted in a greater mineral absorption due to their larger soil colonization and exploration capacity. This finding has also been evidenced by Harman et al. (2004) while observing the effects of Trichoderma species, or by Ferus et al. (2019), who described a higher root growth in red oak seedlings inoculated with the

Fig. 11.1 Main mechanisms involved in the increase of nutrient uptake by endophyte-infected plants

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endophyte Beauveria bassiana (Bals.-Criv.) Vuill. On the other hand, Lledó et al. (2015, 2016) observed genus Penicillium and Chaetosphaeronema increased the total root biomass in Poa pratensis, and Chaetosphaeronema, Sordaria fimicola, and Epicoccum nigrum exhibited a similar effect in Trifolium subterraneum. Studies performed by Bartholdy et al. (2001) and Johnson et al. (2013) stated the enhacement of Fe uptake in plants growth and development. One of the mechanisms of such an effect might be due to the production of siderophores, which strongly bind Fe3+ . This is supported by the fact that several endophytic fungi, such as species of Epichloë/Neotyphodium, contain a non-ribosomal peptide synthetase gene (sidN) encoding a siderophore synthetase (Johnson et al. 2013). Earlier, Altomare et al. (1999) reported the secretion of siderophores by endophyte Trichoderma harzianum Rifai, increasing Fe uptake by their host plants. In general, nutrient uptake in plants through roots is mediated, among others, by mass flow, and/or root interception (Jungk 2002). Mass flow takes place when nutrients are transported to root by the movement of water in the soil, hence any modification in the above or below ground biomass in a plant could affect the nutrient acquisition (White et al. 1997). In plants with a more proliferation of roots, mass flow tends to increase corresponding to increased nutrients uptake due to the presence of endophytic fungi. This fact was reported by Soto-Barajas et al. (2016) in a study conducted with Epichloë endophytes, wherein N, Ca, Mg, S, Mn, and Mo increased in endophyte-infected plant, Lolium perenne. Root interception occurs when nutrients play physical contact with the root surface and thus when a plant-endophyte interaction stimulates larger root biomass, root interception might be positively altered. This interaction can also modify rhizosphere conditions, affecting the presence, survival, or development of different rhizospheric organisms, which in turn may facilitate nutrient uptake (Antunes et al. 2008; Liu et al. 2011; Omacini et al. 2006). Nutrient transfer between many plant-fungal symbioses is a common strategy, where fungal symbionts facilitate the uptake of soil nutrients by plant hosts, and the plant may supply plant-derived carbohydrates to the developing fungus (Kiers et al. 2011). Under this nutrient-transfer perspective, root-associated endophytes were able to mobilize different nutrients via fungal hyphae, thus helping plants in their nutrient uptake (Behie and Bidochka 2014). Usuki and Narisawa (2007) found that the endophyte Heteroconium chaetospira (Grove) Ellis, transfered N to Chinese cabbage plants, and Newsham (2011) stated that Phialocephala fortinii transfered both, N and P from soil to plant roots via fungal hyphae, thus an increase in minerals concentration occurred in plant roots and shoots. Similarly, studies conducted with the ascomycete root-inhabiting endophyte, Colletotrichum tofieldiae (Pat.), demonstrated their role to facilitate the transfer of P to non-mycorrhizal plant hosts via their hyphae (Almario et al. 2017; Hiruma et al. 2016). This fact is especially interesting for plants growing in nutrient-limited conditions. Studies conducted with the fungal endophyte Piriformospora indica Sav. showed its capacity to induce a normal growth of maize plants cultivated under nutrient-stress conditions, by facilitating the transfer of P from soil to plant roots (Yadav et al. 2010). Chen et al. (2013) observed Phomopsis liquidambari causing growth promotion, nitrification, and NH4+ –N release. Further, the fungal endophyte P. indica has been reported stimulating the expression of the

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gene encoding nitrate reductase, activating also the uptake of trace elements (Mo, B, Fe, Zn, and Mn) in the rhizosphere (Su et al. 2016, 2019). The higher nutrient uptake in endophyte-infected plants occurred due to the endophytic borne secretion of substances that facilitate the mineral uptake by plant roots. In this scenario, Curvularia geniculata (Tracy and Earle) Boedijn has been found to secrete enzymes exhibiting P solubilization in sufficient amounts so as to enhance plant growth and development (Priyadharsini and Muthukumar 2017). On the other hand, the release of root exudates containing some phenolic compounds secreted by Epichloë endophytes, were found to increase the P solubility in soil, increasing the P uptake and the subsequent P concentration in the plants (Malinowski et al. 1998). Similar studies have also reported an increased capability to bind Cu in the rhizosphere of endophyte-infected plants (Malinowski et al. 2004). Increment of P and other mineral solubilization occurred due to the secretion of substances by root endophytes which acidifies the soil, thus P becomes more available in the soil solution by its conversion from insoluble phosphates or other insoluble fertilizers (Aciego and Brookes 2009; Narsian and Patel 2000). Special mention deserves (DSE) which have been found to make mineral nutrients available by facilitating access to complex C, N, and P present in the soil for their host plant (Mandyam 2008). Such an effect could be explained by the production of hydrolytic enzymes by the endophyte, which could induce the release of nutrients to be uptaked by plants. Long back, Jumpponen and Trappe (1998) reported the uptake of organic compounds (amino acids, small peptides, etc.) by DSE fungi, which might be transferred directly to host plants, resulting in more efficient use of organic nutrient resources (Reeve et al. 2008). As stated earlier, DSE and mycorrhizal fungi establish a kind of symbiosis with several plant taxa, where hyphae grow endophytically in roots, extending their mycelia into the soil, to acquire nutrients and to mobilize them to plants (Marschner and Dell 1994). Thus, interactions between DSE and host plants improved plant fitness due to an increment in the N and P transfer and uptake, and nutrient provision to host plants (Gasoni and De Gurfinkel 1997; Usuki and Narisawa 2007). A few of these mechanisms are summarized in Table 11.2. Most of these results have been found to be considerably variable depending on the host plant, fungal strains, and environmental conditions (Haselwandter and Read 1982; Jumpponen 2001; Svenningsen et al. 2018). Thus varying results are obtained under different environmental conditions as observed in rice with Phomopsis liquidambari, where analyzing the transcript levels of several genes in endophyte-infected tissues, it was found that the genes with higher transcript levels, OsAMT1;1, OsAMT1;3, OsAMT2;2, OsAMT3;2, OsAMT3;2 and Os- NRT2;1 increased under low-N conditions (Li et al. 2018).

11.4 Plant Growth Under Alleviation of Stress Conditions The accumulation of mineral salts in soils has become nowadays one of the most serious and growing environmental problems in arid and semi-arid areas causing

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Table 11.2 Summary of the main mechanisms that affect the nutrient absorption by endophyteinfected plants Mechanism of action

Endophyte species

Plant host

Reference

–

Harman et al. (2004)

Neotyphodium coenophialum

Festuca arundinacea Schreb

Assuero et al. (2006)

Chaetosphaeronema sp.

Poa pratensis L.

Lledó et al. (2015)

Chaetosphaeronema sp.

Trifolium subterraneum L.

Lledó et al. (2016)

Sordaria fimicola

Trifolium subterraneum L.

Lledó et al. (2016)

Epiccocum nigrum

Trifolium subterraneum L.

Lledó et al. (2016)

Epichloë festucae

Lolium perenne L.

Soto-Barajas et al. (2016)

Beauveria bassiana

Quercus rubra L.

Ferus et al. (2019)

Trichoderma harzianum

–

Altomare et al. (1999)

Phialocephala fortinii

–

Bartholdy et al. (2001)

Epichloë festucae

Lolium perenne L.

Johnson et al. (2013)

Neotyphodium occultans

Lolium multiflorum L.

Omacini et al. (2006)

Neotyphodium coenophialum

Festuca arundinacea Schreb

Antunes et al. 2008

Neotyphodium lolii

Lolium perenne L.

Liu et al. (2011)

Heteroconium chaetospira

Brassica rapa ssp. pekinensis (Lour.) Hanelt

Usuki and Narisawa (2007)

Piriformospora indica

Zea mays L.

Yadav et al. (2010)

Phialocephala fortinii

–

Newsham (2011)

Metarhizium sp.

Phaseolus vulgaris L.; Panicum virgatum L.; Glycine max L.

Behie and Bidochka, (2014)

Colletotrichum tofieldiae Serendipita indica

Arabidopsis thaliana L.

Hiruma et al. (2016); Almario et al. (2017)

Curvularia geniculata

Cajanus cajan L.

Priyadharsini and Muthukumar (2017)

Neotyphodium coenophialum

Festuca arundinacea Schreb

Malinowski et al. (1998)

Plant root growth Trichoderma sp. promotion

Production of siderophores

Interaction with rhizospheric microorganisms

Nutrient interception via hyphae

Release of root exudates

(continued)

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Table 11.2 (continued) Mechanism of action

Endophyte species

Plant host

Reference

Aspergillus aculeatus

–

Narsian and Patel (2000);

Neotyphodium sp.

Lolium perenne L.

Malinowski et al. (2004)

Periconia macrospinosa; Microdochium sp.

Grasses and crops

Mandyam (2008)

severe physiological stress, and thus reducing the growth and yield of different crops (Ruiz-Lozano et al. 2012). Salt accumulation into soil reduces the osmotic potential of water, which reduces consequently the nutrient and water uptake by plant roots (Porcel et al. 2016). Phomopsis indica confers salt tolerance to plants by increasing the uptake of nutrients such as N, P, and Ca, or improving K +/Na+ homeostasis (Waller et al. 2005). This action, according to Ghorbani et al. (2019) is regulated by the expression of NHXs, SOS1, and CNGC15 genes, maintaining water status through the regulation in the expression of aquaporins, and diminishing the negative effects of salinity stress. Similarly, Epichloë coenophiala caused a better osmotic adjustment of the grass tiller meristems in infected tall fescue plants during periods of drought, allowing plants a quicker growth after the end of the drought period (Elmi and West 1995). On the other hand, metal pollution in soils has dramatically increased during the last few decades. It is expected to continue in the future, causing important losses in the biodiversity and environmental sustainability (Rozp˛adek et al. 2018). Consequently, through soil–plant interaction, in addition to the negative effects caused by plant fitness and growth, toxic metals accumulate in the food chain, arising severe risks for both human and animals. Under such situation, any investigation aiming to reduce the uptake of toxic metals in plant-degraded lands ecosystem might be really welcome. Deng and Cao (2017) indicated that metal availability for plants is governed by the pseudo-equilibrium between aqueous and solid soil phases rather than by the total metal content. They stated that interactions between root exudates and soil components can prevent the increase of water-soluble organo-metallic chelates in the rhizosphere, suggesting that the organic compounds exuded by roots/microbes rapidly absorbed into soil. With this action, a reduction in water-soluble pools of metals occurred for their availability in plants. Rhizosphere usually suffers changes in biochemical, chemical, and physical properties when compared with the rest of the soil, as a consequence of the release of rhizodeposits by roots and/or the secretion of some chemicals by microbes living in the root zone or adjacent soil (Kumar et al. 2013). In general, rhizosphere microorganisms can increase solubility or change the speciation of metals and metalloids by producing organic ligands. This fact is regulated via microbial decomposition of soil organic matter, exudation of metabolites, and microbial siderophores that can form complex cationic metals or desorb anionic species by ligand exchange. Microbes may immobilize metals such as Cd,

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Cu, Zn, etc., by controlling soil pH (Wenzel 2009). In this context, eukaryotes are more sensitive to metal toxicity in comparison to that of prokaryotes, i.e. bacteria, and their typical mechanisms to regulate metal concentration is the expression of some metal-chelating proteins such as metallothioneins (Durán et al. 2011). The easiest mechanisms for the endophytes to regulate metal uptake by plants could be explained by the extracellular immobilization and/or cell wall binding. Thus, Green and Clausen (2003) observed the use of chelators in immobilizing metals in the soil. Such chelators are mainly organic acids as citrate and oxalate, easily created by fungi (Marina et al. 2019; Odoni et al. 2017). Bilal et al. (2018) co-inoculated Sphingomonas and Paecilomyces formosus and bacteria Sphingomonas sp. in soybean plants; an improvement was observed in plant growth under Al and Zn stresses. The inhibition in the metal uptake and translocation resulted in the enhancement of the nutrients uptake caused by the endophyte and modulate soil extracellular enzymatic activities. Ikram et al. (2018) found the IAA producer endophyte Penicillium roqueforti to increase the uptake of several nutrients, showing a low concentration of heavy metals in shoot and roots when allowed to grow in wastewater. This increase in nutrients uptake by plants growing in contaminated soils was mainly due to their association with endophytes (Khan et al. 2010), which increased the solubility of the nutrients of the soil. DSE fungus Exophiala pisciphila, can accumulate Pb and Cd up to 20% and 5% dry weight, respectively, in the roots (Zhang et al. 2008). This fact is especially interesting in pasture species growing in metal-polluted soils because the accumulation might take place in roots, remaining the aerial part of these plants thus, acted as safe feed to the animals. Thus, the poisoning by lead of the cattle, which is the most reported cause of poisoning in farm livestock (Suttle 2010), might be, at some extent, avoided. Inoculation with Mucor sp. in some plants of Brassicaceae in degraded soils due to heavy metals (van der Ent et al. 2013; Verbruggen et al. 2009) resulted in lower metal accumulation in plant tissues. Facilitating metal transport from the cytosol into the vacuole help in increasing metal tolerance of its plants (Rozpadek et al. 2018). Always depending on the interaction of the symbiont with the environmental conditions (Ahlholm et al. 2002), a large number of fungal endophytes induce growth and development in polluted soils that occurred due to the removal of heavy metals as summarized in Table 11.3. Various workers (Dennis et al. 1998; Soleimani et al. 2010; Soto Barajas et al. 2016) reported that endophytes can be considered as a solution for cropping in heavy metal-polluted areas. Likar and Regvar (2013) showed that Phialophora endophytes allowed Salix plants to live and grow normally in Cdpolluted soils due to the decrease in the metal uptake. Reductions in the Cu uptake by plants were also reported by Zabalgogeazcoa et al. (2006), while Monnet et al. (2001) and Malinowski and Belesky (1999) indicated a decrease of Cu and Al uptake by plants. Lledó et al. (2015, 2016, 2017) reported the endophytic fungus Stemphylium globuliferum to cause a dicrease in the Al content in the aerial biomass of legumes and in the Cr concentration in herbage of P. pratensis when cultivated in greenhouse conditions. However, field experiments with the same endophyte in subterranean clover showed an increase in the Al content in aerial biomass of the plant (Lledó et al. 2016). More consistent results were obtained in case of endophyte Fusarium

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Table 11.3 Plant growth enhancement under stress conditions mediated by endophytic fungi Stress source

Mechanism

Endophyte species

Plant host

Reference

Piriformospora indica

Oryza sativa L.

Porcel et al. (2016)

Regulation in the expression of aquaporins

Piriformospora indica

Solanum lycopersicum L.

Ghorbani et al. (2019)

Drought tolerance

Osmotic adjustment of the grass tiller meristems

Epichloë coenophiala Festuca Waller et al. arundinacea Schreb (2005)

Waste water

Secretion of IAA; Lower concentration of heavy metals

Penicillium roqueforti Triticum aestivum L.

Ikram et al. (2018)

–

–

Khan et al. (2010)

Heavy metals accumulation as Fusarium oxysporum nanoparticles within intracellular spaces

–

Durán et al. (2011)

Al

Stemphylium globuliferum

Trifolium subterraneum L.

Lledó et al. (2016)

Fusarium lateritium

Trifolium subterraneum L.

Lledó et al. (2016)

Stemphylium globuliferum

Ornithopus compressus L.

Lledó et al. (2017)

Fusarium lateritium

Ornithopus compressus L.

Lledó et al. (2017)

Phialophora sp.

Salix sp.

Likar and Regvar (2013)

Salt tolerance Nutrient uptake increase; K +/Na+ homoeostasis improvement

Contaminated Increase in the soils nutrient solubility of the soil

Mineral uptake decrease

Cd

Mineral uptake decrease

Cd and Pb

Root accumulation Exophiala pisciphila

–

Zhang et al. (2008)

Facilitating metal transport from the cytosol into the vacuole

Brassicaceae

van der Ent et al. (2013); Verbruggen et al. (2009)

Mucor sp.

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lateritium, which caused a decrease in the Al concentration in the aboveground biomass in both greenhouse and field conditions (Lledó et al. 2016). The high Al content in forage is not desirable due to the antagonistic metabolism of Al and P, and the negative effects of Al on lambs’ appetite (Krueger et al. 1984). These findings may allow the use of the forage produced in soils with a high concentration of Al by the livestock more safely.

11.5 Conclusion Although not many studies have exclusively dealt with the enhanced capacity of fungal endophytes-infected plants for nutrients uptake, the available literature revealed promising results in this field. Thus, fungal endophytes have been proved to be a suitable strategy to increase nutrient uptake and to reduce soil metal pollution or salinization due to anthropogenic activities or climate change. Several mechanisms have been proposed for the enhancement of nutrient uptake in the plant caused by endophytes. The secretion of siderophores to bind Fe, the solubilization of P to make it more absorbable by root, or the transport of N via hyphae from soil to roots are well documented. Besides, fungal endophytes can secrete compounds favoring the chelation of heavy metals into soil, avoiding their uptake by plants, as well as the accumulation in the mycelia to help plants living in polluted soils. These findings are considered to resolve the issue of lowering the plant sustainability by the involvement of endophytes in plant nutrients uptake.

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Chapter 12

Endophytic Rhizobacteria for Mineral Nutrients Acquisition in Plants: Possible Functions and Ecological Advantages Becky Nancy Aloo, Vishal Tripathi, Ernest R. Mbega, and Billy A. Makumba

Abstract Nutrient-deficiency in agricultural soils is a major problem in many parts of the world, it is, therefore, artificial fertilizers are widely used to boost crop production. Unfortunately, these fertilizers are associated with a myriad of environmental problems hence, there is a need for viable alternatives. The realization that the plant microbiome can improve plant health, soil fertility, and crop productivity is one of the most fascinating scientific discoveries in the world. For several decades, rhizobacteria have been studied due to their various plant growth-promoting (PGP) traits. Endophytic rhizobacteria are unique plant microbiome that establish themselves within plant root tissues and exert beneficial functions to their hosts without harming them. A lot of emphases have been put on these bacteria as viable tools for sustainable agriculture and it is advanced that they could be better plant growth promoters than their external counterparts. However, this theory is not yet clearly understood. This chapter provides the current state of understanding of the putative functions of endophytic rhizobacteria and their future prospects for plant mineral nutrients acquisition. Their advantageous traits that largely advanced to facilitate these PGP functions are also discussed. Such informations can provide better opportunities for improved plant mineral nutrients acquisition and enhance the application of these microbes as viable strategies for sustainable agriculture. Keywords Endophytes · Rhizobacteria · Sustainable agriculture · Plant growth promotion B. N. Aloo (B) · E. R. Mbega Department of Sustainable Agriculture and Biodiversity Conservation, Nelson Mandela African Institution of Science and Technology, P. O. Box 447, Arusha, Tanzania e-mail: [email protected] B. N. Aloo Department of Biological Sciences, University of Eldoret, P. O. Box 1125-30100, Eldoret, Kenya V. Tripathi Institute of Environment and Sustainable Development, Banaras Hindu University, P. O. Box 221005, Varanasi, UP, India B. A. Makumba Department of Biological Sciences, Moi University, P. O. Box 3900-30100, Eldoret, Kenya © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_12

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12.1 Introduction Agricultural activities are quickly gaining momentum to feed the rapidly growing population across the globe. One of them is excessive use of chemicals established as an effective tool to increase crop productivity of different crops. However, conventional agricultural practices have a lot of undesirable outcomes as the chemical inputs have commonly been linked to land degradation, environmental pollution, global warming, climate change, etc. (Steffen et al. 2015; Di Benedetto et al. 2017). For many decades, researchers all over the world have focused on alternative crop fertilization mechanisms such as the use of plant growth-promoting bacteria (PGPB) to replace the contemporary fertilization practices (Smith et al. 2016). In fact, these are free-living bacteria with unique capabilities of stimulating plant growth, either directly or indirectly through different mechanisms (Archana et al. 2013; Ahemad and Kibret 2014; Kumar et al. 2014). Glick (2014) and later, Baliyan et al. (2018) described the exploitation of such organisms as a viable and environment friendly technology befitting for sustainable crop production in eco-safe ways. Among them, endophytes are organisms that spend all or part of their lives in plant cells or tissues with different degrees of dependence without harming their hosts (Compant et al. 2010; Hardoim et al. 2015; Brader et al. 2017; Lata et al. 2019) and can be recovered from surface-sterilized plant tissues (Santoyo et al. 2016). As many plant species as exist on earth host bacterial endophytes (Ryan et al. 2008), and several endophytic bacteria like the Proteobacteria, Firmicutes Actinobacteria, and Bacteroidetes have putative PGP functions (Rosenblueth and Martinez-Romero 2006; Bulgarelli et al. 2013; Hardoim et al. 2015; Liu et al. 2017). Endophytic bacteria have been isolated from various plant parts including stems, roots, seeds, leaves, fruits, ovules, tubers, nodules, etc. (Benhizia et al. 2004; Pandey et al. 2018). Nevertheless, below ground potential i.e., plant roots harbor the greatest populations of these bacteria in comparison to aerial parts (Rosenblueth and Martinez-Romero 2006; Taghavi et al. 2010), at approximately 104 –106 per g of root tissue (Compant et al. 2010; Bulgarelli et al. 2013). Depsite occupying different ecological niches, endophytic bacterial populations employ PGP mechnaisms similar to those of free-living rhizosphere bacteria (Compant et al. 2005). The common PGP mechanisms can either be direct such as nitrogen-fixation, solubilization of nutrients, production of siderophores and phytohormones or indirect such as the suppression of plant pathogens and diseases (Suman et al. 2016; Lata et al. 2018). Diverse PGP bacterial endophytes have been explored and applied for crop yield enhancement under nutrient-poor conditions (Rosenblueth and Martinez-Romero 2006; Liu et al. 2017). Several studies demonstrate their positive effects in different food and cash crops such as the banana (Musa spp.) (Patel et al. 2017b), maize (Zea mays) (Alves et al. 2015), tomato (Lycopersicon esculentum) (Upreti and Thomas 2015), groundnut (Arachis hypogaea) (Dhole et al. 2016), and many more outlined by various workers (Hardoim et al. 2015; Pandey et al. 2018; Maheshwari 2018). Literature documents that endophyte-elicited PGP activities culminate into increased seed germination rates, biomass, chlorophyll, N

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and protein contents, root and shoot lengths, yield, and tolerance to abiotic stresses (Verma et al. 2013, 2015). The rhizobia which are the best-understood endophytes are critical for Nitrogen (N) nutrition in leguminous plants (Santoyo et al. 2016). Although endophytic rhizobacteria have widely been investigated, their significance in improving plant mineral nutrient acquisition has emerged quite recently (Harman and Uphoff 2019), and literature propounds that they could be better plant growth promoters and possess certain advantageous traits that give them an edge over their external counterparts (Coutinho et al. 2015; Asaf et al. 2017). However, this theory is not yet clearly understood as both are similar to their facilitation of plant mineral nutrients acquisition. This chapter reviews the potential functions of endophytic rhizobacteria in the acquisition of certain plant mineral macronutrients such as N, P, K and micronutrients like Zn and Fe. The putative advantageous traits that facilitate these functions and make them suitable candidates for enhancing mineral nutrients acquisition in plants are also discussed. Such information will enrich our knowledge on these important plant endophytic microbiome and possibly pave the way for their complete understanding and utilization as biofertilizers for sustainable crop production.

12.2 Putative Functions of Endophytic PGPR for Mineral Nutrients Acquisition in Plants Several studies demonstrate the diversity and functions of endophytic rhizobacteria toward plant mineral nutrients acquisition and general PGP activities. In this section, we outline some of these studies and functions to demonstrate the importance of these bacteria in plant mineral nutrition.

12.2.1 Endophytic Rhizobacteria and Nitrogen Acquisition in Plants Nitrogen is the most important nutrient required for plant growth (Verma et al. 2019). Although the atmosphere contains about 78% N, most of this is present in inert form and inaccessible to plants, making it a major plant-limiting nutrient. Artificial Nfertilizers are commonly applied to supply N to plants. However, out of every 100 Tg of N applied in agricultural fields globally, only about 17 Tg are utilized by plants and the rest is either lost or accumulates in the environment with serious implications to the soil and environment (Erisman et al. 2008; Howarth 2008). The microorganisms can convert excess ammonium or nitrate in the soil into nitrous oxide (N2 O), a potent greenhouse gas (GHG) (Kandel et al. 2017), whose effects are reportedly much worse than that of CO2 (Ramaswamy et al. 2001).

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Endophytic N2 -fixing rhizobacteria are now emerging as one of the most efficient and environmentally sustainable approaches for increasing N acquisition for crops (Suman et al. 2016; Defez et al. 2017). Their potential has been illustrated in many studies, examples of which are provided in Table 12.1. It is proposed that endophytic N2- fixers can enable plants to survive under N-limiting conditions better than their external rhizobacterial counterparts (Gupta et al. 2013). For instance, the N2 fixation process requires energy to reduce the bonds in the N2 molecules and the endophytic N2- fixers can obtain the required energy from plant host tissues (Olivares et al. 2013). Similarly, their internal plant habitats offer favorable micro-aerobic environments that are more conducive to the nitrogenase enzyme complex that catalyzes the N2 fixation process (Doty et al. 2016). Although all diazotrophs are important for providing N to plants and enhancing their growth (Kumar et al. 2017), endophytic rhizobacteria not only provide the fixed N to their plant hosts more directly but also more efficiently (Suman et al. 2016; Lata et al. 2019). This is because the BNF process is largely mediated by the nif and fix genes whose transcriptions are primarily induced under low-oxygen conditions as in the interior plant tissues parts that host the endophytes (Bhagya and Rajkumar 2017). Literature suggests that the fixed N2 is converted to NH4 + in the bacterial cytoplasm and subsequently excreted into the host cytoplasm (Mia and Shamsuddin 2010), where it is assimilated into glutamate and transported in the xylem from the plant roots to their shoots as the major source of organic N (Nawaz et al. 2017). Thus the endophytic diazotrophs can release NH4 easily and directly into the plant host cell cytoplasm. Although some N2 -fixers can assimilate the produced NH4 into organic compounds, most N2 -fixing strains have unique regulatory mechanisms to secrete the NH4 outside their cells by diffusion instead of assimilating it (Day et al. 2001). This has a significant implication on the utilization of rhizobacteria as biofertilizers since the absence of this negative feedback mechanism can allow the nitrogenase enzyme complex to produce NH3 continuously for plant uptake. The symbiotic N2 -fixing rhizobia inhabiting in the cortial tissues of roots have been researched for several decades (Santoyo et al. 2016). The inoculation of crops and agricultural fields with such PGPR can help to maintain the N levels (Daman et al. 2016). For instance, about 1–2 kg N ha−1 day−1 can be obtained for all legumes by rhizobial N2 fixation alone (Lesueur et al. 2016). Apart from legumes, rhizobia have also been found living endophytically with rice, sweet corn, cotton, maize, bean, barley, and wheat among others as outlined in the review by Bhagya and Rajkumar (2017). This shows that there is a great possibility that several rhizobial interactions can similarly enhance N acquisition with non-leguminous crops. For instance, the discovery of N2 -fixing endophytic rhizobacteria in sugarcane (Ohyama et al. 2014; Mus et al. 2016) and cereals (Annapurna et al. 2004; Suman et al. 2016) especially sparked a substantial interest. Rhizobia have also been found to infect Brassica campestris and enhance its growth by increasing its N content (Chandra et al. 2007). Gluconacetobacter diazotrophicus which is the main endophytic diazotroph in sugarcane can fix up to 150 kg N ha−1 year−1 (Muthukumarasamy et al. 2005), and previous in vivo studies on this species also showed that it can promote the growth, germination, height, and nutrient uptake of sugarcane (Suman et al. 2008). Recently, a study

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Table 12.1 Some important nitrogen-fixing endophytic rhizobacteria and their associated host plants Source

Endophytic rhizobacteria

Reference

Banana (Musa spp.)

Klebsiella sp., Bacillus sp., Microbacterium sp., Enterobacter sp.,

Patel et al. (2017b)

B. subtilis

Andrade et al. (2014)

Cassava (Manihot esculenta)

Pantoea dispersa

Chen et al. (2014)

Cowpea (Vigna unguiculata)

Bradyrhizobium, Streptomyces griseoflavus

Htwe et al. (2019)

Groundnut (Arachis hypogaea)

Enterobacter ludwigii

Dhole et al. (2016)

Bradyrhiziobium

Taurian et al. (2013)

Maize (Zea mays)

Pseudomonas aeruginosa, E. asburiae, Acinetobacter brumalii

Sandhya et al. (2017)

Klebsiella sp., K. pneumoniae, B. pumilus Acinetobacter Kuan et al. (2016) sp., B. subtilis Bacillus sp., Enterobacter sp.

Szilagyi-Zecchin et al. (2014)

P. pseudoalcaligenes, P. aeruginosa

Jha (2019)

Mungbean (Vigna radiata)

Bradyrhizobium, Streptomyces griseoflavus

Htwe et al. (2019)

Rice (Oryza sativa)

Microbacterium, Bacillus, Klebsiella spp. Paenibacillus Ji et al. (2014) kribbensi, B. aryabhattai, K. pneumoniae, B. subtilis, M. trichotecenolyticum Rhizobium

Patel et al. (2017a)

Burkholderia, Herbaspirillum, Azospirillum, Rhizobium leguminosarum

Choudhary and Kennedy (2004), Doty (2011)

P. stutzeri

Pham et al. (2017)

Lysinibacillus sphaericus

Shabanamol et al. (2018)

Rhizobium sp., Azospirillum sp.

Sev et al. (2016)

Soybean (Glycine max)

Bradyrhizobium, Streptomyces griseoflavus

Htwe et al. (2019)

Sugarcane (Saccharum officinarum L)

Gluconacetobacter diazotrophicus

Suman et al. (2008)

Pantoea agglomerans

Quecine et al. (2012)

K. variicola DX120E

Wei et al. (2014) (continued)

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Table 12.1 (continued) Source

Endophytic rhizobacteria

Reference

G. diazotrophicus

Ahmed et al. (2016)

Kosakania sp. ICB117

Kleingesinds et al. (2018)

Wheat (Triticum Achromobacter insolitus, Azospirillum brasisilense aestivum) Stenotrophomonas maltophilia, Chryseobacterium, Flavobacterium, Pseudomonas mexicana

Silveira et al. (2016) Youseif (2018)

involving other endophytes in a mixed inoculum also showed increased N uptake in sugarcane under N-limiting conditions (Marcos et al. 2016), an implication that there could be other beneficial diazotrophs in this plant. Ngamau et al. (2014), reviewed a number of endophytic banana rhizobacteria with BNF potential. As evidenced by these studies and many others, diazotrophic endophytes hold immense potential for enhancing N acquisition in various non-leguminous plants and further investigations in this regard are necessary.

12.2.2 Endophytic Rhizobacteria and Potassium Acquisition in Plants Potassium is the third most important quality macronutrient required for plant metabolism and growth (Ahmad et al. 2016; Proença et al. 2017). However, over 90% of K occurs in soil in fixed forms and only about 2% is readily available for plant use (Tsegaye et al. 2017; Meena et al. 2018). The application of K-based/potash fertilizers is a contemporary practice in extensive and intensive agricultural systems worldwide (Dasan 2012; Yagedari et al. 2012; Zhang et al. 2013). However, these synthetic fertilizers decrease agricultural profitability (Mohammadi and Sohrabi 2012; Ahmad et al. 2016) and sustainable crop yield. Potassium solubilizing bacteria (KSB) are an important source of the rhizosphere microbiome where they promote plant growth by solubilizing K-bearing minerals. Recent literature shows that KSB can be used to ameliorate K-deficient soils for crop production (Suman et al. 2016; Dhiman et al. 2019), and are quickly gaining momentum in the wake of calls for sustainable crop production (Ahmad et al. 2016). The burgeoning evidence of the large diversity of KSB associated with different plants shows that they have an immense potential for application in K-deficient soils (Meena et al. 2016; Velázquez et al. 2016). However, K solubilization abilities are less reported among endophytic rhizobacteria (Proença et al. 2017; Dhiman et al. 2019). For instance, in a study by Patel et al. (2017b), none of over 50 endophytic banana rhizobacteria were associated with K solubilization despite them showing

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other essential PGP functions including the solubilization abilities for other important plant nutrients. Nevertheless, there are studies that demonstrate the existence of K solubilizing endophytes. Potassium solubilizing endophytic rhizobacteria have been identified from wheat (Verma et al. 2013, 2015), more recently, from pearl millet (Kushwaha et al. 2019), maize (Jha 2019), and other crops (Dhiman et al. 2019). Rhizobia are the best-studied endophytes and are widely known for symbiotic N2 fixation in leguminous plants (Santoyo et al. 2016). However, of late, these novel rhizobacteria have also been shown to solubilize K in plant rhizospheres. For instance, K solubilization by rhizobia in rice has recently been reported by Patel et al. (2017a). Thirumal et al. (2017) demonstrated 5 rhizobial cultures associated with K solubilization in vitro. These new discoveries suggest that apart from enhancing N nutrition in plants, rhizobia can also be exploited for their K solubilizing abilities to enhance K availability in plant rhizosphere. Indigenous KSB are currently in the limelight for sustainable cropping systems and environmental conservation and have emerged as one of the viable technologies for mitigating K-deficiency in soils (Meena et al. 2015). Potassium solubilization indeed holds a lot of potential for PGP and the K solubilizing abilities of endophytic rhizobacteria are worth exploring. According to Meena et al. (2018), KSB are precious bio-resources that can mitigate K-deficiency in agricultural soils but their experimental evidence at the field level is still inadequate. Such processes may need to be exploited in detail so as to increase their usability.

12.2.3 Endophytic Rhizobacteria and Phosphorus Acquisition in Plants Phosphorus is the second most important plant nutrient after N (Goswami et al. 2016). Although soils contain P reserves, most of this is available in insoluble forms and inaccessible to plants (Verma et al. 2019). This non-availability is recognized as a major plant growth-limiting factor in agricultural systems (Sharma et al. 2013). The P solubilization potential of soil microorganisms is one of the most essential traits of PGPR for enhancing P-nutrition acquisition in plants (Walia and Shirkot 2012; Ouattara et al. 2019). While P solubilizing rhizobacteria are widely investigated, recent literature maintains that only a few endophytic rhizobacteria possess this ability (Brigido et al. 2019). Nevertheless, there is mounting evidence on the role of endophytes in P solubilization and mobilization compared to their widely reported rhizospheric counterparts (Ji et al. 2014; Oteino et al. 2015; Walitang et al. 2019). PSB can proliferate both in plant rhizospheres and endosphere (Hui et al. 2011), and according to Suman et al. (2016), P solubilization is a common trait among endophytic bacteria. However, the P solubilizing bacteria (PSB) still tend to be more abundant in plant rhizospheres in comparison to plant cells and tissues (Chen et al. 2006; Mwajita et al. 2013; Mehta

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et al. 2015; Walia et al. 2017). Generally, the population of endophytic PSB range between 102 and 104 bacteria/g of root tissue (Kumar et al. 2013; Saini et al. 2015). A number of endophytic rhizobacterial populations belonging to Burkholderia, Enterobacter, Pantoea, Pseudomonas, Citrobacter, Azotobacter genera from wheat, rice, maize, legumes, and sunflower, respectively, are reported to solubilize mineral P in plate assays, and a vast number of P solubilizing PGPR are documented (Verma et al. 2013, 2015). In a recent study, Patel et al. (2017b), examined that 36% of over 50 endophytic rhizobacterial isolates belonging to genera Bacillus, Klebsiella, Microbacterium, and Enterobacter showed P solubilization. Further reports on P solubilizing endophytic rhizobacteria are depicted in Table 12.2. The P solubilizing PGPR can greatly impact plant growth by increasing P availability in the rhizospheric soils but must maintain an intimate relationship with the host plants (Walia et al. 2017). Numerous studies have highlighted the importance and mechanisms of P solubilization by PSB (Chhabra and Dowling 2017; Varma et al. 2017; Walia et al. 2017; Shrivastava et al. 2018; Billah et al. 2019; Goswami et al. 2019; Rafi et al. 2019; Dheeman et al. 2020). The solubilization of P is purportedly mediated through acidification, chelation, or exchange reactions (Li et al. 2017). According to Rosenblueth and Martinez-Romero (2006), endophytic PSB are more competitive than free-living rhizobacteria since the plant-endophyte interactions are the result of complex evolutionary processes. Moreover, endophytic rhizobacteria can prevent the adsorption and fixation of P under P-limiting conditions by assimilating the solubilized P (Khan and Joergersen 2009; Shakeela et al. 2017).

12.2.4 Endophytic Rhizobacteria in Zinc Acquisition in Plants Zinc is an important micronutrient required for primary and secondary metabolism in plants (Goteti et al. 2013; Bhatt and Maheshwari 2020). For instance, Zn is a cofactor in many enzymes (Hafeez et al. 2013) and it is critical for membrane function, photosynthesis, protein synthesis, and auxin metabolism in plants (Tavallali et al. 2010). Reports show that Zn deficiency is a common problem worldwide due to nutrient mining during crop harvesting and increased use of NPK fertilizers containing lesser amounts of Zn micronutrients (Sharifi and Paymozd 2016; Sindhu et al. 2019). Synthetic Zn fertilizers are often applied to overcome these deficiencies at rates of about 25 kg ha−1 ZnSO4 heptahydrate (equivalent to 5 kg ha−1 Zn). Nevertheless, these artificial fertilizers are not cost-effective and quickly get converted into insoluble forms that are inaccessible to plants (Bapiri et al. 2012; Sindhu et al. 2019). Rhizobacterial Zn solubilization abilities are widely reported phenomenon (Mishra et al. 2013; Shaikh and Saraf 2017). Reports also exist on endophytic Zn solubilization. For instance, Zn solubilizing bacteria (ZSB) have been reported to enhance Zn uptake in soybean up to 21% (Sharma et al. 2014), various G. diazotrophicus strains showed solubilization potential for various Zn compounds (Suman et al. 2016)

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Table 12.2 Studies demonstrating phosphate-solubilization by endophytic rhizobacteria in different crops Source

Endophytic rhizobacteria

Reference

Bananas (Musa spp.)

B. subtilis, Agrobacterium tumefaciens, Streptomyces sp., B. thuringiensis, B. amyloliquefaciens, Micrococcus luteus

Matos et al. (2017)

B. subtilis, Lysinibacillus sp.

Andrade et al. (2014)

Black pepper (Piper nigrum)

Klebsiella sp., Enterbacter sp.,

Jasim et al. (2013)

Cassava (Manihot esculenta)

Pantoea dispersa

Chen et al. (2014)

Chickpea (Cicer arietinum)

B. subtilis, B. licheniformis

Saini et al. (2015)

Bacillus sp., Klebsiella sp., Pseudomonas sp.

Chhabra and Sharma (2019)

P. agglomerans, B. cereus, B. sonorensis

Maheshwari et al. (2019a)

Cocoa (Theobroma cacao)

Not determined

Ouattara et al. (2019)

Common bean (Phaseolus vulgaris)

Pseudomonas sp.

Dini´c et al. (2014)

Common pea (Pisum sativum)

P. agglomerans, B. cereus, B. sonorensis

Maheshwari et al. (2019a)

Tumeric (Curcuma longa L.)

B. cereus, B. thuringiensis, B. pumilis, P. putida, Calvibacter michiganensis

Kumar et al. (2016)

Faba bean (Vicia faba L.)

Rhizobium nepotum, R. tibeticum

Rfaki et al. (2015)

Ginseng (Panax ginseng)

Lysinibacillus fusiformis, B. megaterium, B. cereus Vendan et al. (2010)

Maize (Zea mays)

Bacillus spp., Klebsiella sp., E. ludwigii, Pantoea spp.

de Abreu et al. (2017)

P. aeruginosa, E. asburiae, Acinetobacter brumalii Sandhya et al. (2017) Klebsiella sp., K. pneumoniae, B. pumilus Acinetobacter sp. and B. subtilis

Kuan et al. (2016)

Non-identified species

Manzoor et al. (2017)

P. pseudoalcaligenes, P. aeruginosa

Jha (2019)

Peach (Prunus persica) Brevundimonas diminuta, Agrobacterium tumefaciens, Stenotrophonomas rhizosphilia

Liaqat and Eltem (2016)

Peanut (Arachis hypogaea)

Taurian et al. (2013)

P. agglomerans

(continued)

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Table 12.2 (continued) Source

Endophytic rhizobacteria

Reference

Pearl millet (Pennisetum glaucum)

Bacillus spp.

Ribeiro et al. (2018), Kushwaha et al. (2019)

Potato (Solanum tuberosum L.)

Bacillus spp., Pseudomonas spp., Serratia spp.

Abd El-Moaty et al. (2018)

Rice (Oryza sativa)

Paenibacillus kribbensi, B. aryabhattai, K. pneumoniae, B. subtilis, Microbacterium trichotecenolyticum

Ji et al. (2014)

Serratia sp., Pseudomonas sp.

Yasmin et al. (2016)

B. subtilis, B. megaterium

Dias et al. (2009)

Strawberry (Fragaria ananassa)

Soybean (Glycine max) E. sakazakii, P. straminae, Acinetobacter calcoaceticus

Kuklinsky-Sobral et al. (2004)

Sugarcane (Saccharum Herbaspirillum spp., Bacillus spp. Silva et al. (2015) officinarum L) Burkholderia mallei, B. cepacia, Proteus vulgaris, Awais et al. Pasteurella multocida, K. pneumoniae, K. oxytoca, (2019) E. cloacae, C. freundii Gluconacetobacter diazotrophicus

Crespo et al. (2011)

Tea (Camellia sinensis Bacillus, Brevibacterium, Paenibacillus, L.) Lysinibacter

Borah et al. (2019)

Tomato (Solanum lycopersicum)

Lysinibacillus spp.

Sahu et al. (2018)

Wheat (Triticum aestivum)

Stenotrophomonas maltophilia, Chryseobacterium, Youseif (2018) Flavobacterium, P. mexicana

Wild mint (Mentha arvensis)

Non-identified strains

Batool and Iqbal (2018)

Bacillus sp.

Prakash and Arora (2019)

and the endophytic G. diazotrophicus inhabiting sugarcane have shown to possess Zn solubilization abilities alongside other multifarious PGP activities (Saravanan et al. 2007; Natheer and Muthukkaruppan 2012). Yaish et al. (2015), isolated endophytic bacteria from the date palm tree (Phoenix dactylifera L.), identified as P. aeruginosa, P. monteilii, P. putida, Acitenobacter brumalii, E. asburiae, Sinorhizobium meliloti, P. thivervalensis, P. fulva, and P. lini were capable of solubilizing Zn oxide (ZnO). The Gram-positive B. aryabhattai was also shown to improve the growth of soybean and wheat due to Zn solubilizing processes (Ramesh et al. 2014). Investigations on rhizobial and Pseudomonas cultures demonstrated the in vitro solubilization of different forms of insoluble Zn (Thirumal et al. 2017). The ability to solubilize various sources of insoluble Zn

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has been emphasized in the selection of potential endophytes for enhancement of Zn uptake in plants (Singh et al. 2018). Other endophytic ZSB include species of Bacillus, Chryseobacterium, Paenibacillus, Rhodococcus, Staphylococcus, Achromobacter, Acinetobacter, Enterobacter, and Klebsiella (Suman et al. 2016). Recently, Kushwaha et al. (2019) also observed that endophytic Bacillus strains from pearl millet exhibited Zn solubilization potential and had multiple roles in stress tolerance of the plant. The use of such ZSB can increase Zn uptake by filed crops, which would in turn lead to their improved growth and yield (Suman et al. 2016).

12.2.5 Endophytic Rhizobacteria and Iron Acquisition in Plants Iron is the fourth most abundant element in soil and is an important micronutrient required by plants for many physiological processes (Saha et al. 2016). However, most agricultural soils are Fe-deficient because the element occurs in the insoluble ferric (Fe3+ ) form that is unavailable for plant uptake (Rajkumar et al. 2010; Arora and Verma 2017; Singh et al. 2019). Some microorganisms have developed a special Fe acquisition mechanism under these Fe-limiting conditions by producing certain special metabolites known as siderophores (Maheshwari et al. 2019b). Siderophores are secondary metabolites with high affinity for Fe3+ (Goswami et al. 2016; Arora and Verma 2017), and under Fe-limiting conditions, siderophores complex with Fe3+− , a phenomenon which is important for enhancing Fe availability in the rhizosphere (Ferna´ndez-Scavino and Pedraza 2013; Boiteau et al. 2016; Chhabra and Dowling 2017). It is proposed that once the siderophores bind onto Fe3+ , the acquisition of the bound Fe by plants can occur by the degradation of the chelates or complexes (Rajkumar et al. 2009). According to Loaces et al. (2011), siderophore production is a common trait among the free-living PGPR (Souza et al. 2015) and is rarely reported for the endophytic rhizobacteria. Recent literature suggests that only a few endophytic bacterial isolates possess this trait (Brigido et al. 2019), investigated mainly as a bio-control agent against plant pathogens (Suman et al. 2016). In such cases, the siderophores chelate most of the Fe present in the rhizosphere and prevent the proliferation of pathogens due to its non-availability in the rhizosphere soil (Mitter et al. 2013; Olanrewaju et al. 2017). Nevertheless, endophytic rhizobacteria can also produce these metabolites under Fe-stress and aid in plant Fe acquisition (Ghavami et al. 2017; Perez-Rosales et al. 2017), and endophytic genera like Pantoea, Bacillus, Burkholderia, and Pseudomonas can increase the concentration of bioavailable Fe in plant tissues (Maheshwari et al. 2019a). Endophytic siderophore producers that include Brevundimonas diminuta, Leifsonia shinshuensis, Sphingomonas parapaucimobilis, Brevundimonas vesicularis, and Agrobacterium tumefaciens have been identified from pear and peach roots (Liaqat and Eltem 2016). Bacillus sp., Pseudomonas sp., and Stenotrophomonas sp. are also recognized among the effective siderophore-producing endophytes (Jasim

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et al. 2014). Serratia sp. and Pseudomonas sp. from rice have been recently reported to produce siderophores by Yasmin et al. (2016). Siderophore-producing endophytic P. agglomerans from peanuts (Taurian et al. 2013), and in turmeric (Kumar et al. 2016) have also been reported. The endophytic Bacillus sp. and P. putida were also associated with siderophore production. Similar studies on pepper endophytic Paenibacillis polymyxa by Phi et al. (2010) also exhibited such abilities by Vendan et al. (2010). The endophytic bacteria such as B. cereus, B. flexus, B. megaterium, Lysinibacillus fusiformis, L. sphaericus, Microbacterium phyllosphaerae, Micrococcus luteus isolated from maize also showed excellent siderophore production. Investigations by Youseif (2018) also demonstrated siderophore production capabilities by wheat-root endophytic Stenotrophomonas maltophilia, Chryseobacterium sp, Falvobacterium sp., and Pseudoxanthomonas mexicana. In another study, Maheshwari et al. (2019b), characterized siderophore-producing endophytic bacteria from chickpea (Cicer arietinum) and pea (Pisum sativum). Earlier, Wani and Khan (2010) stated that chickpea endophytic Pseudomonas sp. was one of the dominant siderophore-producing genera of the plant. Patel et al. (2017b), observed endophytic rhizobacterial isolates identified as Bacillus, Klebsiella, Microbacterium, and Enterobacter species which showed excellent siderophore production abilities. Similarly, siderophore-producing endophytes have also been isolated from maize and canola (Ghavami et al. 2017), corn (Szilagyi-Zecchin et al. 2014), banana, etc. (Ouma et al. 2014). Siderophore-producing endophytes are important to crops not only directly by improving Fe availability for plant uptake but also indirectly by depriving Fe required to plant pathogens (Chhabra and Dowling 2017; Aloo et al. 2019b). The completed genome analyses of endophytic microbes like Enterobacter species have shown that they contain a large number of genes that code for siderophore transporter proteins (Taghavi et al. 2010). The production of siderophores is a classic example of how rhizobacteria can improve Fe availability in the plant rhizosphere and due to its indisputable role in plant nutrition, further investigations on siderophore-producing rhizobacteria are necessary (Aloo et al. 2019a).

12.3 Ecological Significance of Endophytes in Mineral Nutrients Acquisition by Plants Endophytic rhizobacteria are considered as sub-sets of rhizosphere microbiome that have acquired the ability to colonize plant root tissues and exhibit specialized and unique lifestyles (Compant et al. 2010; Dheeman et al. 2017). Despite their special interaction with plants, endophytes share all the important PGP traits with other rhizobacteria (Compant et al. 2005). However, they possess characteristics that are distinct from rhizospheric bacteria, suggesting that not all rhizospheric bacteria can enter plants, and/or that once inside their hosts, they change their lifestyles to adapt to internal habitats within plants (Monteiro et al. 2012; Sessitsch et al.

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2012). For instance, a study on plant colonization and the establishment of symbionts by Hardoim et al. (2015) showed the presence of significant putative properties in endophytes compared to other types of bacteria interacting with plants. There is an increasing interest in harnessing the potential of endophytic microbes to develop sustainable crop production systems. Although endophytic rhizobacteria are considered a subset of the rhizospheric microflora, their endophytic lifestyle offers them a myriad of advantages over rhizospheric growth (Compant et al. 2010). For instance, they establish themselves in sheltered micro-environments within the plant root tissues (Castanheira et al. 2017), which are protective ecological niches that provide them with safe, consistent, and undisturbed environments as opposed to external rhizobacteria (Senthilkumar et al. 2011). Literature advances that endophytic microbes are relatively protected from external biotic and biotic environmental stresses, unlike their external counterparts whose survivability and colonizability are largely dependent on extrinsic soil factors (Rajkumar et al. 2009; Suman et al. 2016; Waghunde et al. 2017; Lata et al. 2019; Dubey et al. 2020). Living endophytically allows these bacteria to maintain close contact with plant root tissues for the direct and constant supply of nutrients and their beneficial effects can be exerted onto the host plants more directly (Lata et al. 2019). The plant endosphere niche presents a unique habitat, and bacterial endophytes possibly have differential functions, specializations, adaptations, and competence (Compant et al. 2010). The diversity of endophytic communities also varies depending on host plant species and genotypes, location, developmental stages, and local environmental conditions (Shi et al. 2014). Nevertheless, the direct and intimate interactions that endophytic rhizobacteria form with plant root tissues makes them highly valuable tools and suitable candidates for improving mineral nutrient acquisition in plants more directly and efficiently (Sreejith et al. 2019).

12.4 Conclusions and Future Prospects The need for eco-friendly crop fertilization alternatives is increasingly becoming urgent. However, endophytic rhizobacteria have not been fully understood and the prospects of finding unique and interesting bacteria are great. Identifying endophytic rhizobacterial strains with multiple PGP functions for specific plants can definitely pave way for more benefits in terms of plant mineral nutrients acquisition. As such, present and future research work should focus on the largely unexplored rhizobacterial endophytes and their potential uses for mineral nutrients acquisition in plants (Turner et al. 2013). Most plant-endophyte interactions have involved rhizobia and legumes and future research should explore fresh alternatives on their application for other agronomically important crops (Suman et al. 2016). Although there is a wealth of information on culture-dependent and independent characterization of endophytic rhizobacterial diversity and their associated in vitro PGP mechanisms, reports on their practical applications as plant inoculants under

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field conditions are extremely scarce (Liu et al. 2017). Several endophytic rhizobacteria have been identified in laboratory studies but generally fail to give consistent results under field conditions and there is need to understand the complex dynamics that control plant-endophyte associations probably by identifying genes that govern these relationships at the molecular level. Although some studies have been conducted in this area, they remain limited and genomic analyses can decipher into the capabilities of endophytes and their roles in plant mineral acquisition. Our knowledge about the plant-microbe interactions can greatly be enhanced using metabolomic, genomic, and transcriptomic methods (Dubey et al. 2020). At the moment, only a limited number of genes that contribute to endophytic invasion and colonization have been identified. Perhaps whole-genome sequencing of these organisms will facilitate the identification of novel isolates and their successful exploitation for plant mineral nutrients acquisition. Further analysis of the sequenced genomes and characterization of the involved genes can also help to improve our understanding of their interaction with plants (Compant et al. 2010) for full exploitation. These efforts can also lead to the identification of some new genes required for endophytic lifestyle but there would be a need to separate the common genes for rhizosphere colonization from those involved in the endophytic lifestyle. Additionally, a more comprehensive understanding of whether these organisms are likely to establish themselves in plants if applied as biofertilizers is needed (Compant et al. 2010). Numerous reports have revealed a range of beneficial features of the endophytic rhizobacteria for plant mineral nutrients acquisition. Nevertheless, there is still a great scope of further exploration and identification of more novel functions. For instance, research on N2 fixation and P solubilization abilities by endophytic plant rhizobacteria continues to expand, but very little strides have been made regarding K solubilization yet K is the third major essential macronutrient for plant growth. Similarly, limited work has been carried out on S-oxidation (Dhiman et al. 2019). A combination of both traditional and modern biotechnological methods will help in advancements toward improved plant mineral nutrients acquisition and sustainable agriculture (Waghunde et al. 2017). Although a broad range of endophytes with traits for enhancing mineral nutrient acquisition in different plants have been described, only a few of these have conclusively been studied to demonstrate their significance in plants (Chhabra and Dowling 2017). Furthermore, the impact of endophytic colonization and enhanced nutrient uptake in plants can be varied depending on plant host species/cultivars, endophyte strains, and environmental conditions (Shi et al. 2014). The successful manipulation of the plant microbiome can substantially contribute to sustainable agricultural production (Bakker et al. 2012; Tkacz et al. 2015), by reducing the need for chemical inputs (Adesemoye et al. 2009; Kandel et al. 2017) and GHG emissions (Singh et al. 2010). This chapter provides a comprehensive review of the putatie functions and ecological significance of endophytic PGPR for mineral nutrient acquisition in plants. Taking into consideration the intimate relationships they form with their plant hosts, these rhizobacteria present special tools for improving plant mineral nutrients acquisition and could be better plant growth promoters than their external counterparts (Lata et al. 2019). Endophytes are

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indeed fascinating life forms and there is no doubt that their intricate lifestyles and plant interactions still require better understanding to facilitate their application as viable alternatives to artificial fertilizers for agricultural sustainability.

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Chapter 13

Plant Growth-Promoting Bacteria: Effective Tools for Increasing Nutrient Use Efficiency and Yield of Crops Chitra Pandey, Shrivardhan Dheeman, Deepti Prabha, Yogesh Kumar Negi, and Dinesh Kumar Maheshwari Abstract Agrochemicals or fertilizers are essential to optimize crop production but their excessive and unwanted application is posing a myriad of adverse effects such as declining soil fertility besides contaminating surface and groundwater. These synthetic chemicals mismanage the soil ecology leading to disturbed ecosystem and loss of beneficial bacteria inhabiting in soil. Traces of such chemicals have also been deposited in agricultural products that cause serious illnesses in human beings. Considering such facts, the use of plant growth-promoting bacteria (PGPB) renamed as plant beneficial bacteria being promoted to enhance nutrient availability, plant growth, and yield promotion to maintain sustainable agriculture. These bacteria have been in use for a long time for increasing plant growth and development and to reduce the subsistence farmer’s dependence on agrochemicals. The scientific community observed that beneficial effects are now befitting for the sustainable growth promotion and crop yield enhancement due to the influence of PGPR in order to augment nutrient uptake capacity and nutrient use efficiency. The aim of the present study is focusing on the PGPRs which work as a tool to enhance nutrient use efficiency of various crops. Long-term application of such bacteria could act as a newer alternative to C. Pandey Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala, India e-mail: [email protected] S. Dheeman Department of Microbiology, School of Life Sciences, Sardar Bhagwan Singh University, Balawala, Dehardun, India S. Dheeman · D. K. Maheshwari Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India D. Prabha Department of Seed Science and Technology, Chauras Campus, HNB Garhwal University, Srinagar, Uttarakhand, India Y. K. Negi (B) Department of Basic Sciences, College of Forestry (VCSG UUHF), Ranichauri, Tehri Garhwal, Uttarakhand, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_13

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chemical fertilizer and able to cope its adverse effects on both soil and ecology and reverse plant–soil ecosystem. Keywords PGPR · Crop yield · Rhizosphere · Nutrient management

13.1 Introduction Agriculture has been and will continue to be the backbone of food availability and food security. It directly sustains the livelihood of about two-third of the global population, and is the lifeline of agro-industries. However, over time, the sustainability of agricultural growth has emerged as a central issue confronting many countries in the world. This issue has become even more important as the pressure on land and other natural resources has increased manifold with an increase in population and per capita consumption of food grains (Negi 2005). As the world population is dwelling, food availability has to be increased corresponding to meet out the increasing food demand. The current world population of 7.6 billion and is expected to reach 8.6 billion in the year 2030 and 9.8 billion in 2050 (UNDESA 2017). Therefore, the use of agrochemicals has become important to sustain agriculture production and fulfill the food requirement of all human beings worldwide. Initially, the use of these chemicals was much promoted among the farmers to grow the crops at their best. However, their long-term headforemost application results in low soil fertility and increases the dependency of farmers on these agrochemicals. Farmers use a variety of agrochemicals and depend on them for the successful production of their crops. Another constraint of agriculture production is decreasing land availability for farming. This will further lead to the enhancement of nutrient load per unit area in soil. The depletion of nutrients in the soil is, therefore resulting in poor plant growth and productivity. Plants require 16 essential nutrients or elements for adequate growth and production. Three of these, carbon (C), oxygen (O), and hydrogen (H) are drawn from water and the air. The remaining elements are taken up from the soil (Gellings and Parmenter 2016). These nutrients have been divided into three categories viz. macronutrients, micronutrients, and trace elements (Table 13.1). Crop health and productivity depend on the availability of these nutrients and their uptake as well. However, this is well known that most of the nutrients in the soil are present in complex or unavailable forms. Inorganic fertilizers are thus manufactured in plant-available forms. Therefore, as these fertilizers are amended in soil, the nutrients get quickly released and become available for plant uptake. Fertilizers undoubtedly increase productivity and fulfill the food demand but, at the same time, their adverse effects on soil, environment, and human beings increase many-fold. Unfortunately, residual accumulation of these harmful chemicals in grains, fruits, and other edible parts has been reported in recent years by many researchers (Bhanti and Taneja 2007; Gurusubramanian et al. 2008; Singh et al. 2008). Consumption of such contaminated produces may cause serious health problems (e.g., allergic reactions, intestinal disorders, hormonal imbalance, and even cancer) in human beings

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Table 13.1 Plant nutrients and their role S.

Nutrient types

Element

Role in plant growth

no. 1.

Macronutrients Nitrogen (N) (Required in large quantities and their deficiency or unavailability affect plant survival) Phosphorous (P)

Potassium (K)

2.

3.

Micronutrients Calcium (Ca) (Required in fewer amounts and their deficiency or unavailability may result in poor plant health and low productivity)

The basic component of proteins and chlorophyll. Plays an essential role in plant growth Plays an important role in root growth and promotes the establishment of young plants, flowering, fruiting and ripening, photosynthesis, respiration, and overall plant growth Promotes the movement of sugars, turgor, and stem rigidity. It also increases the plant’s overall resistance to cold, diseases, insect pests, etc. Promotes the formation of flower buds, the hardening off of woody plants, and fruiting It plays a vital role in plant structure because it is part of cell walls and holds them together. Promotes the development of the root system and the ripening of fruit and seeds. Also, found in the growing parts of plants (apex and buds)

Magnesium (Mg)

An important part of chlorophyll. Helps in fruit ripening and seed germination. Reinforces cell walls and promotes the absorption of phosphorous, nitrogen, and sulfur by plants

Sulfur (S)

A component of several proteins, enzymes, and vitamins. Contributes to chlorophyll production. It helps plants absorb potassium, calcium, and magnesium

Trace elements Iron (Fe) (Required in very fewer amounts and their deficiency or unavailability may result in poor metabolic functions, health, and Boron (B) low productivity)

Essential for chlorophyll production. It also contributes to the formation of some enzymes and amino acids Essential to overall plant health and tissue growth. Promotes the formation of fruit and the absorption of water (continued)

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Table 13.1 (continued) S.

Nutrient types

Element

Role in plant growth

Manganese (Mn)

Promotes seed germination and speed-up plant maturity. Plays an important role in photosynthesis by contributing to chlorophyll production. Essential for nitrogen assimilation and protein formation

no.

Molybdenum (Mo) Essential for nitrogen assimilation by plants and nitrogen fixation by bacteria. This means that it is needed for the production of nitrogen-based proteins Chlorine (Cl)

Stimulates photosynthesis

Copper (Cu)

Activates various enzymes. It also plays a role in chlorophyll production

Zinc (Zn)

Plays an important role in the synthesis of proteins, enzymes, and growth hormones

(Bhanti and Taneja 2007; Singh et al. 2008). Another side of the coin is that the fertility of the soil has decreased over time resulting in decreased productivity due to deprived soil nutrients. So many chemicals are there in use to control pests, insects, and pathogens with an instant effect. However, irrelevant and indiscriminative use of these chemicals is leading to a very harmful effect on human health (Lawrence et al. 2004; Chaturvedi et al. 2013), soil environment (Aktar et al. 2009; Lin et al. 2019; Tiryaki and Temur 2010), and animals (Dalvie et al. 2011; Odukkathil and Vasudevan 2013). It is well known that (i) these chemicals are recalcitrant and not fully degradable, and (ii) their degradation depends on their half-life, the amount applied, chemical reaction, etc. (Pandey et al. 2017). All these factors have arisen questions among the scientific community, environmentalists, and social organizations regarding food security, soil, water, and air pollution, crop nutrition, soil fertility, etc. These problems provoked the scientific community to search for environment-friendly commercial alternatives that could act as good as chemicals to increase soil fertility and crop productivity to ensure food security. A large number of publications have appeared during the last decade on the use of plant growth-promoting bacteria (PGPR), organic manures, botanicals, etc., and come up as a vivacious and viable alternative to agrochemicals. Such biological alternatives not only enhance the nutrient availability but also increase their uptake by host plants. Besides this, PGPRs secrete plant

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growth hormones, antibacterial and antifungal metabolites, induce systemic resistance against many diseases and thereby ensure higher crop production and another advantage of these microbes is that they can be applied with other biological inputs.

13.1.1 Organic Manures: An Alternative Source of Plant Nutrients Generally, plant and animal residues or by-products come under this category such as compost, manure, and animal residues. Being organic, these fertilizers have a good amount of different nutrients and therefore increase soil fertility (Li et al. 2018). Unlike inorganic chemicals, these fertilizers do not show any harmful effects on plants or human beings. Also, they are biodegradable, renewable, and sustainable. However, beneficial microorganisms help in the adequate release of nutrients in the soil from these fertilizers. Their strategic use may not only enhance the crop production but also improves the soil quality and fertility. Organic manures viz., FYM, vermicompost, poultry compost, cattle dung, etc., improve the physical properties of soil (water hold-ing capacity, soil aeration, soil aggregation, etc.), prevent soil degradation and increase the population of beneficial soil microorganisms. These organic amendments contain most of the nutrients in a plant-available form such as nitrates, phosphates, exchangeable calcium, zinc, and soluble potassium (Orozco et al. 1996). Similarly, forest litter also plays a fundamental role in nutrient turnover and the transfer of energy between plants and soil. This is also a good source of the nutrients that are accumulated in the upper layers of the soil. FYM is used in between 10 and 30 t ha−1 in different crops including cereals, pulses, vegetables, etc. Vermicompost and Forest litter are used 6–10 t ha−1 . However, the rate of application of organic manures can be reduced if applied along with microbial inoculants biofertilizers. Several reports suggest a 25–50% reduction in organic manure requirements if beneficial microbes are combined with them (Yildrim et al. 2011; Singh et al. 2015; Rahman et al. 2018).

13.2 Plant Growth-Promoting Bacteria Although, much has been said about PGP bacteria (Maheshwari 2011; Maheshwari et al. 2015, 2017) it is pertinent to give a brief description about their role and efficacy. Plant growth-promoting rhizobacteria (PGPR) are the beneficial bacteria closely associated with plant rhizosphere and possess plant growthpromoting abilities (Kloepper and Schroth 1978). These are used to improve soil fertility and crop productivity and also as biocontrol agents to reduce crop losses. To commemorate their spectrum of action, they are designated with several terms

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including plant growth-promoting bacteria, plant health-promoting bacteria, bioinoculant, biofertilizers, biocontrol agents, etc. PGPRs generally represent a wide range of root colonizing bacteria belonging to Azotobacter, Azospirillum, Bacillus, Burkholderia, Rhizobium, Pseudomonas, Serratia, etc. Along with plant growth promotion, they reforest eroded areas, restore the contaminated sites, and thereby render a positive effect on the degraded soil ecosystem (Gupta et al. 2015). It seems inevitable that fewer agrochemicals with their low dosages will be used in the coming time and more emphasis would be put on the use of environmentally and biologically safe alternatives including the use of beneficial microbes. PGPRs have been found successful in getting established in the soil ecosystem due to their high adaptability in a wide variety of environments, faster growth rate, and biochemical versatility to metabolize a wide range of natural and xenobiotic compounds. Successful studies using PGPRs including genera Acinetobacter, Alcaligenes, Arthrobacter, Azospirillum, Azotobacter, Bacillus, Burkholderia, Caulobacter, Chromobacterium, Enterobacter, Erwinia, Flavobacterium, Micrococcus, Rhizobium, Serratia, Xanthomonas, Proteus, and Pseudomonas on the growth enhancement of various crops have been achieved in laboratory and field conditions (Glick 1995; Gray and Smith 2005; Verma et al. 2010; Negi et al. 2011; Maheshwari et al. 2015; Agarwal et al. 2017b) in Table 13.2. PGPRs produce growth hormones, enzymes, and other metabolites that facilitate solubilization of soil nutrients (phosphate, nitrogen, potassium, etc.) and thereby enhance nutrient uptake with subsequent augmentation of the plant growth (Baligar et al. 2001; Mishra et al. 2009). The interaction between plant, soil, and microbes is influenced by abiotic (physical, chemical) and biotic (soil biota) factors (Jackson and Prat 1996; Putten et al. 2013). Abiotic factors such as temperature (low and high), high salt, pH, soil fertility, moisture content have been reported to influence enzyme activities nutrient, concentration (Chapin 1980), and nutrient uptake (Gavito et al. 2001) which have shown to affect plant growth directly or indirectly (Heinze et al. 2017). Plant growth-promoting bacteria secrete various phytohormones such as GA (Bottini et al. 2004; Hayat et al. 2010), IAA (Spaepen et al. 2007), Cytokinin, Salicylic acid (Jochum et al. 2019), abscisic acid (Cohen et al. 2015). Phytohormones like auxins, cytokinins, and gibberellin production have been observed for the significant enhancement of seedling parameters (Melnykova et al. 2013; Talboys et al. 2014). The broad spectrum antagonistic activities of PGPRs are executed by secretion of several metabolites including antibiotics (Guo et al. 2014; Lee et al. 2016), volatile compound HCN (Khabbaz et al. 2015), siderophores (Kesaulya et al. 2018), enzymes chitinase and β-1, 3-glucanase, etc. (Huang et al. 2005). These beneficial microbes can easily be applied in different crops by seed, root treatments, foliar sprays, mixing in soil or organic manure, etc., to various crop plants (Fig. 13.1). The demerits include (i) requirements for long-term storage, and (ii) generally crop-specific or site-specific.

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Table 13.2 Different PGPR strains found effective to increase plant growth of various crops S. no.

Bacterial strains used

Crop

References

1.

Pseudomonas fluorescence (ATCC13525)

Vigna radiata

Katiyar and Goel (2004)

2.

Pseudomonas putida (B0)

Zea mays var. QPM-1

Pandey et al. (2006)

3.

Serratia marcescens SRM (MTCC 8708)

Curcurbita pepo

Selvakumar et al. (2007)

4.

Serratia marcescens SRM

Triticum sp. cv. VL 802 Selvakumar et al. (2008)

5.

Acinetobacter rhizosphaerae BIHB 723

Pisum sativum var. Palam priya, Zea mays var. Girija, Hordeum vulgare var. Dolma

Gulati et al. (2009)

6.

Pseudomonas spp.

Triticum aestivum L.

Mishra et al. (2011)

7.

Pseudomonas fluorescence

Phseolus vulgaris var Pusa contendor

Negi et al. (2011)

8.

Rhizobium, Pseudomonas, Serratia, Bradyrhizobium japonicum-SB1, Bacillus thuringiensis KR1

Lens culinaris Medikus Kaur et al. (2015)

9.

Pseudomonas sp. JJS2, Enterobacter sp. AAB8

Cajanus cajan (L.) and Shukla et al. Eleusine coracana (2015)

10.

Rhizobium sp.

Lentil (Lens culinaris Medikus)

Singh et al. (2018)

11.

Bacillus subtilis and B. pumilus

Amaranthus hypochondriacus

Pandey et al. (2018a, b)

13.2.1 Potential Role of Microbes in Nutrient Availability Plant growth-promoting bacteria are known for their ability to increase nutrients concentration in rhizospheric and non-rhizospheric soil. PGPR can increase phosphorus, nitrogen, potassium, and other micronutrients concentration in the soil (Vejan et al. 2016). These nutrients are in unavailable form in the soil and PGPR achieve availability of these by solubilization, due to siderophore production and oxidation of sulfur, etc. A significant amount of nitrogen (from 20 to 22 TgN per year up to 40 Tg N per year) has been contributed to the agriculture system due to N-fixation (Galloway et al. 2008; Herridge et al. 2008). Other nutrients such as Fe and Zn are also required to increase plant growth, and PGPR increases the availability by using different mechanisms. Zn mobilizing bacteria have been observed to increase Zn uptake along with the crop yield (Ramesh et al. 2014; Shakeel et al. 2015). The isolation, identification, and characterization of Zn and K solubilizing bacteria

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Fig. 13.1 Effects of PGPR applications on plants

have been reported. Along with that PGPR (Microbacterium oxydans JYC17, Pseudomonas thivervalensis Y1-3-9, and Burkholderia cepacia J62) having metal resistance increased Cu uptake (maximum 113.38%) by Rape plant and improved copper remediation capacity and also increased antioxidant content in leaves, the biomass of remediation plant (Ren et al. 2019). Canbolat et al. (2006) reported a significant effect of Bacillus M-13 and Bacillus RC01 on nitrogen fixation and phosphate solubilization and increased availability promotes the uptake of these nutrients by barley (Hordeum vulgare). In another case, Maize plant grew on nutrient-deficient calcisol soil when treated with the Pseudomonas alkaligenes PSA15, Bacillus polymyxa BcP26, and Mycobacterium phlei MbP18, improved soil nutrients and uptake of the nutrients (N, P, K), was observed. Bacterial inoculants have been observed as a better plant growth promoter in nutrient-deficient soil (Egamberdiyeva 2007). Strains of Pseudomonas fluorescens, Pseudomonas putida, and Pseudomonas fluorescens were found effective to increase nutrient uptake and field in paddy (Lavakush et al. 2014). Recently, Pandey et al. (2018a) reported that biopriming of amaranth seeds by the selected Bacillus isolates exhibited a significant increase in all three macronutrients (N: 36.18%, P: 32.45%, K: 17.11%) in soil. Authors also reported that the higher solubilization and availability of these nutrients significantly increased the grain yield in Amaranthus hypochondriacus.

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13.2.2 Nutrient Use Efficiency (NUE) Nutrient use efficiency reflects the ability of a plant to use the available nutrients at its maximum potential. It can be defined as yield (biomass) per unit input of fertilizer/nutrient content). NUE, therefore, depends on the plant’s ability to take up nutrients efficiently from the soil but also depends on internal transport, storage, and remobilization of nutrients. NUE is a critically important concept for evaluating crop production systems and can be greatly impacted by fertilizer management (Baligar et al. 2001). It is classified into four different subtypes (i) Agronomic efficiency, (ii) Physiological efficiency, (iii) Apparent recovery efficiency, (iv) Utilization efficiency as described in Table 13.3 (Baligar et al. 2001). Nutrient use efficiency of chemical fertilizers is very low which ultimately leads to increased fertilizer amount in the field and subsequently, that remaining fertilizer vanished in the environment. Even if fertilizer could apply in an adequate amount, plants use only 50% and the remaining 50% leached out in the environment, for instance, plant uptake 50% of nitrogen fertilizer and remaining polluting water (Chandini et al. 2019). Since plants primarily depend on soil for all their nutrients, it is important to make them available in a utilizable form. Different nutrients have their specific role in plant growth and development and therefore, must be available at the required concentration. By the application of agrochemicals, farmers try to amend the soil with sufficient nutrients. Therefore, it is necessary to manage the nutrient application Table 13.3 Types of Nutrient use efficiency S. no. 1.

Type of nutrient use efficiency Physiological efficiency (PE)

Definition and description Physiological efficiency is defined as the Yield F (kg) Yield C (kg) Nutrient uptake F (kg)

Nutrient uptake C (kg)

Where Yield F is the biological yield of a fertilized plot (kg), Yield C is the biological yield of an unfertilized plot (kg), Nutrient uptake F is nutrient uptake of a fertilized plot (kg), Nutrient uptake C is nutrient uptake of an unfertilized plot (kg) 2.

Agronomic efficiency (AE)

Grain Yield F (kg) Grain Yield C (kg) Quantity of nutrient applied (kg) Agronomic efficiency expressed as the additional amount of economic yield per unit nutrient applied

3.

4.

Apparent recovery efficiency (ARE)

Utilization efficiency (EU)

Source Baligar et al. (2001)

Nutrient uptake F (kg)

Nutrient uptake C (kg)

Quantity of nutrient applied (kg) ARE has been used to reflect the plant’s ability to acquire applied nutrients from the soil Nutrient utilization efficiency was calculated by formula: EU (kg/kg) = PE X ARE

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and also to increase the plant potential to produce more with the recommended dose of fertilizers. This is quite possible by increasing the “Nutrient use efficiency” (NUE) of the plants. It is the key component to enhance crop productivity. Generally, the NUE is crop or variety-specific but, there are reports, which suggest that PGPRs can effectively increase the NUE in different plants, result in higher crop productivity and nutrient quality. Recent research on plant–microbe interaction has revealed that PGPRs affect the ability of host plants to efficiently utilize the absorbed nutrients and increase yield and nutritive quality of the produce (Pandey et al. 2018a, b; Rahman et al. 2018).

13.2.3 PGPRs in NUE Enhancement High crop yield is the result of adequate availability of nutrients in the soil and their optimum uptake and accumulation in the plant systems. This, in turn, may enhance the NUE of the plant. It has been reported that PGPR provides the optimum level of nutrients to the plants and thereby increasing plant growth and yield (Pandey et al. 2018b; Rahman et al. 2018). Usually, nutrients are present in the soil but, generally, they remain in plant unavailable form and PGPRs can convert them into the available form (Adesemoye and Kloepper 2009). PGPR group of bacteria are soluble in nature. Some of the bacterial genera increase soil N, P, and K availability by solubilization and fixation reaction. PGPRs possess different mechanisms for higher nitrogen availability which include ammonification, nitrification, denitrification, mineralization, etc. (Ogunseitan 2005). A diverse range of PGPRs are known to enhance nitrogen use efficiency, for instance, Acetobacter, Azoarcus, Arthrobacter, Azotobacter, Azospirillum, Bacillus, Burkholderia, Enterobacter, Pseudomonas, Nitrobacter, Nitrosomonas, Rhizobium, etc. (Table 13.4). Nitrogen use efficiency is the plants’ ability to utilize available nitrogen in the field to enhance plant growth and productivity. To achieve the best NUE scientific researches were based on 4R principle, i.e., right source, right rate, right time, and right placement. NUE depends on the transport, storage, recycling, remobilization, and plant growth stage along with the nutrient uptake. The synchronization of nitrogen availability with nitrogen demand can increase nitrogen use efficiency significantly. Spolaor and coworkers (2016) suggested consortium of A. brasilense Ab-V5 + V6 and consortium of A. brasilense Ab-V5 and Rhizobium sp 53GRM1 to be effective to enhance the NUE of popcorn and enhanced the grain yield. Zeffa et al. (2019) applied A. brasilense Ab-V5 to improve maize growth and concluded that it increased NUE in N limiting conditions along with the improved root architecture, N assimilation, uptake, and increased biomass. Authors concluded that the morphological and structural changes in the plant occured because of the production of phytohormones by A. brasilense Ab-V5. Ahmad et al. (2017) reported that the PGPR impregnation with the DAP and urea enhanced nitrogen and phosphorus use efficiency of wheat and thereby increased photosynthetic rate, growth, and yield.

Enhancement in nutrient use efficiency. Rice (Oryza sativa) Enhancement in nitrogen use efficiency. Sunflower (Helianthus annuus) Increased N, P uptake and nutrient use efficiency High nutrient uptake and nutrient use efficiency. High nitrogen, phosphorus and potassium uptake, increased nutrient use efficiency. High nitrogen, phosphorus and potassium uptake, increased nutrient use efficiency. Also, high residual availability of nutrients after crop harvest

Burkholderia cepacia RRE25

Pseudomonas aeruginosa QS-40

Bacillus amyloliquifaciens IN937a, Bacillus pumilus T4

Pseudomonas fluorescens, Bacillus megaterium, Azospirillum brasilense

Pantoea agglomerans, Rahnella aquatilis and Pseudomonas orientalis

Bacillus subtilis and B. pumilus

Amaranth (Amaranthus hypochondriacus)

Rice (Oryza sativa)

Maize (Zea maizae)

Tomato (Solanum lycopersicum)

Wheat (Triticum aestivum)

Nutrient uptake

Pseudomonas sp.

Crop

NUE/nutrient uptake

PGPR

Table 13.4 Plant growth-promoting bacteria reported to enhance nutrient use efficiency and nutrient uptake

Pandey et al. (2018b)

Khanghahi et al. (2018)

Gulnaz et al. (2017)

Fan et al. (2017)

Arif et al. (2017)

Singh et al. (2013)

Shaharooma et al. (2008)

Reference

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Wu et al. (2005) evaluated the effect of biofertilizers (AMF, A. chroococcum, B. megaterium, B. mucilaginous) on the maize growth and its nutritional properties and reported enhanced growth, soil properties, and nutritional value (total N, P and K). Increased N and P use efficiency was reported when the wheat plant was treated with P. fluorescens ACC50 and P. fluorescens biotype F (ACC73) (Shaharooma et al. 2008). Arif et al. (2017) observed that the combination of N-enriched compost and P. aeruginosa increased uptake efficiency of a sunflower plant, and a significant difference was observed in seed and quality of oil. Study also revealed that the inoculation of wheat by Azospirillum spp. effectively enhanced P and N use efficiency of wheat along with increased grain yield (Kivi et al. 2014). Ahmad et al. (2017) reported that the combination of PGPRs with a decreased amount of urea and DAP increases plant growth, yield (20%) along with nitrogen, and phosphorus use efficiency of wheat. This can be helpful to heel decreased soil fertility slowly and can add beneficial microbes in the soil. Bacteria in agrobiology have multifarious role including nutrient efficiency in crop plants (Maheshwari et al. 2013). Phosphate solubilizing microbes were found as an effective tool for providing applied nutrients to the rice, few genera, and bean. They increased nutrient uptake (N, P, K) and NUE (Duarah et al. 2011). Those PGPRs having phosphate solubilizing, IAA producing, and disease suppressing ability are known to enhance nutrient uptake and nutrient use efficiency as reported by various workers. According to their study N, P, K uptake, and use efficiency of rice plants increased due to application of hyperproducing IAA mutants of Burkholderia cepacia (RRE25), Bacillus cereus, Brevibacillus reuszeri, and Rhizobium rubi have been reported to increase growth and organic manure use efficiency of strawberry (Karlidag et al. 2009). A concurrent increase in wheat productivity and uptake of N and P was observed by the application of consortium of P. striata, A. chroococcum, and Glomus fasciculatum. Moreover, increased uptake leads to augmented nutrient use efficiency (Khan and Zaidi 2007). PGPRs also influence the micronutrient availability for the plants by using different mechanisms: Root exudates alteration by the symbiotic and non-symbiotic association with their respective host plants; enhancement of soil nutrient availability by increasing the solubility (Adesemoye and Kloepper 2009; Fitter et al. 2011). The plant growth significantly influenced by the micronutrients along with the macronutrients supported metabolic and enzymatic activities in the plant. The effects of PGPRs on nutrient availability and their use efficiency are depicted in Fig. 13.2. In this context, Shabayev (2012) studied the effect of PGPRs and reported increased iron and zinc contents in wheat while Sharma et al. (2015) demonstrated that P. putida and Bacillus sp. BN30 treatment enhanced zinc content rice. Increased Zn content was observed in Jaya and Pusa basmati-1 varieties of rice when treated with Bacillus sp. BN30. Recently, Adak et al. (2016) studied the effect of PGPRs on micronutrient enhancement and reported an increase in iron and zinc content in rice. On the other hand, Pandey et al. (2018b) observed a positive correlation between different treatments and NUE on amaranth using PGP bacilli. The study depicts that NUE of amaranth for N, P, and K were increased with different treatments that would

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Fig. 13.2 Effects of PGPR treatments on nutrient availability, plant growth, and yield

have facilitated their better utilization through different biochemical and metabolic processes to produce higher crop yield.

13.3 Impact on Crop Yield Enhancement PGPRs ameliorate plant health and productivity by enhancing the nutrient status of soil and host plants (Dey et al. 2004). The bioavailability of nutrients and their increased uptake may significantly enhance the nutrient use efficiency of plants. Increased solubilization of nutrients (macro and micro) by PGPRs enhanced their uptake and accumulation (Parmar and Patel 2009; Dhiman et al. 2019; Bhatt and

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Maheshwari 2019). Nutrient availability has been influenced by solubilization, chelation, and oxidation-reduction reaction in soil (de Santiago et al. 2011). Several workers (Puente et al. 2004; Sharma et al. 2012; Prasanna et al. 2013) studied the nutrient enhancement and nutrient availability in the soil as well as in plants that resulted in the bacterial inoculation. Goteti et al. (2013) observed a significant enhancement in nitrogen and phosphorus contents of the maize when inoculated with Bacillus sp. in comparison to that of plants treated with Pseudomonas spp. This implies that PGPRs competence strongly enhanced crop growth with nutrients as well. Han et al. (2006) and Supanjani et al. (2006) applied two species of bacilli, i.e., Bacillus megaterium var. phosphaticum and Bacillus mucilaginosus in nutrient-limited stressed soil where the strains increased bioavailability of minerals, their uptake and thereby enhanced growth of pepper and cucumber. In the same year, Hafeez et al. (2006) suggested the use of Bacillus pumilus as a bioinoculant to promote the crop yield in wheat. Beneduzi et al. (2008) reported Bacillus isolate SVPR30 as an efficient bioinoculant for growth enhancement of the rice. On the other hand, Zongzheng et al. (2010) also evaluated the growth promoter effect of Bacillus subtilis SY1. Their study revealed a significant increase in seedling parameters such as sprout tendency, germination percentage, sprout index, and vigor index. Bacillus isolates exhibited good PGP activities and significantly influenced seedling length, fresh weight, and dry weight of cowpea (Thomas et al. 2010). Bacillus sp. RM-2 was reported to enhance the seedling value parameters of cowpea with an increase in the number of seeds, the weight of seeds, and total grain weight (Minaxi et al. 2011). Agrawal and Agrawal (2013) reported the growth promotion of tomato by Bacillus sp. showing PGP traits. In the same year, Mehta et al. (2015) supported the fact of planting value parameter enhancement by the treatment of bioinoculants. Significant increase in seed germination, shoot length, root length, shoot dry weight, root dry weight, along with an increase in nitrogen, potassium, and phosphorus was observed after the application of Bacillus circulans CB7. Dubey et al. (2014) suggested that the combination of a half dose of chemical fertilizers with the Bacillus BSK17 was effective for the growth promotion of Cicer aerietinum and reported a significant increase in germination, yield. Recently, Refish et al. (2016) accounted for the role of Bacillus subtilis BS87 in the growth promotion of Anoectochilus roxburghii and A. formosanus. Similarly, multifarious bacilli influence was reported to influence the growth promotion of different crops such as Curcuma longa (Chauhan et al. 2016), Fagopyrum esculentum (Agarwal et al. 2017b). Awasthi et al. (2011) recorded enhanced growth and biomass yield of Artemisia annua L. (Asteraceae) when treated with the consortium of Glomus mosseae and B. subtilis. Biocoenotic consortium of P. aeruginosa KRP1 and B. licheniformis was suggested for bioformulation to enhance the productivity of Brassica campestris by Maheshwari et al. (2015). Recently, Vurukonda et al. (2016) evaluated the effect of a consortium of B. cereus, B. subtilis, and Serratia spp. on cucumber plants that exhibited darker green leaves, fewer wilt symptoms increased chlorophyll content and drought resistance. Kumar et al. (2016) suggested consortium of Bacillus spp., Pseudomonas spp., and R. leguminosarum in enhancement for the growth and grain yield of Phaseolus vulgaris. These PGPRs have not only been

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found effective to promote plant growth but also reported to increase soil fertility by solubilizing nutrients in the soil and thereby suggested as an ecofriendly approach toward sustainable agriculture (Bishnoi 2015; Romao-Dumaresq et al. 2017; Singh et al. 2018).

13.4 Conclusion Given the above, it can be concluded that plant growth-promoting bacteria are useful to enhance nutrient availability in soil and nutrient uptake by host plants. If these are used in the long run, they can, therefore, sustain the soil fertility and higher crop yield. The use of potential strains can effectively trigger and enhance the nutrient use efficiency of host plants. The enhanced nutrient use efficiency will not only increase the crop yield but also ensure the sustainable availability of nutrients in the soil even after crop harvest. Such residual amounts may reduce the nutrients quantity required in subsequent crop and thereby will reduce the input cost of the crop. Such strategies can be very effective for the sustainability of crop production and yield essential for food security.

References Adak A, Prasanna R, Babu S, Bidyarani N, Verma S, Pal M, Nain L (2016) Micronutrient enrichment mediated by plant-microbe interactions and rice cultivation practices. J Plant Nutr 39(9):1216– 1232 Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85(1):1–12 Agarwal BD, Broutman LJ, Chandrashekhara K (2017a) Analysis and performance of fiber composites. Wiley, New York, USA Agrawal DPK, Agrawal S (2013) Characterization of Bacillus sp. strains isolated from rhizosphere of tomato plants (Lycopersicon esculentum) for their use as potential plant growth promoting rhizobacteria. Int J Curr Microbiol Appl Sci 2(10):406–417 Agarwal M, Dheeman S, Dubey RC, Kumar P, Maheshwari DK, Bajpai VK (2017b) Differential antagonistic responses of Bacillus pumilus MSUA3 against Rhizoctonia solani and Fusarium oxysporum causing fungal diseases in Fagopyrum esculentum Moench. Microbiol Res 205:40–47 Ahmad S, Imran M, Hussain S, Mahmood S, Hussain A (2017) Bacterial impregnation of mineral fertilizers improves yield and nutrient use efficiency of wheat. J Sci Food Agric 97:11 Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2(1):1–12 Arif MS, Shahzad SM, Riaz M, Yasmeen T, Shahzad T, Akthar MJ, Bragazza L, Buttler A (2017) Nitrogen-enriched compost application combined with plant growth-promoting rhizobacteria (PGPR) improves seed quality and nutrient use efficiency of sunflower. J Plant Nutri Soil Sci 180(4):464–473 Awasthi A, Bharti N, Nair P, Singh R, Shukla AK, Gupta MM, Kalra A (2011) Synergistic effect of Glomus mosseae and nitrogen fixing Bacillus subtilis strain Daz26 on artemisinin content in Artemisia annua L. Appl Soil Ecol 49:125–130

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Chapter 14

Siderophore in Plant Nutritional Management: Role of Endophytic Bacteria Gunjan Garg, Sandeep Kumar, and S. Bhati

Abstract Plants uptake nutrients specifically phosphorus, nitrogen, iron, and potassium with the help of beneficial bacteria in its available form. Bacteria helps in the enhancement of plant growth via direct or indirect ways are considered as a Plant Growth Promoting Rhizobacteria (PGPR). These are green alternatives to conserve soil fertility sustainably by leveraging nutrition supports to plants in many ways. Bacteria also produce siderophores and many phytohormones which support the plant life in adverse stressful conditions. Recently, in this group of bacteria and endophytic fungi many candidates are involved in the production of pyoverdine, hydroxamate, ferrioxamines siderophores in rhizosphere region, which increases three times Iron (Fe) transportation efficiency of root and shoot growth of the plants. Siderophores reflect significant application in metal binding along with the iron and ranked as “Fe-biosensors.” How siderophores production by bacteria facilitate bioremediation, weathering of soil-mineral particles that enhance the plant growth have been reviewed in further. Keywords Siderophore · Phytohormone · Rhizobacteria · Iron deficit soil · Microbiome · Root secretion

14.1 Introduction There is a demand for more yield and production of crops for the food security, while the production rate is adversely affected by different kinds of biotic (insect/pest/fungus, etc.) and abiotic stresses (salt/water/temperature, etc.). Using the biotechnological method, we can contrive transgenic stress tolerance plant, which counterbalances the adverse effects of the environment. Endophytic microbiota plays G. Garg (B) · S. Bhati School of Biotechnology, Gautam Buddha University, Greater Noida 201 308, Uttar Pradesh, India e-mail: [email protected] S. Kumar Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar 249 404, Uttarakhand, India © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_14

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an important role in the host plant’s growth either by the production of secondary metabolite or nutrient assimilation. This helps the plant to adapt themselves to various environmental stresses (i.e., salt and water), an important aspect of crop yields. In the current scenario, enormous knowledge of endophytes, their roles for increasing crop yields, disease-resistant plants, and facilitating the survival under environmental stress is a requirement for the agricultural prosperity. Bacteria, actinobacteria, and some fungi comprise the endophytic microbial system. Endophytic microbiota forms a network surrounding their host plants (Wang et al. 2011; Pahari and Mishra 2017). Generally, they inhabit the intercellular spaces of the host plant. The most common mode of entry for endophytic bacteria into plant tissues is through primary and lateral root cracks, and diverse tissue wounds arising as a result of plant growth (Sprent and de Faria 1998; Agarwhal and Shende 1987; Sørensen and Sessitsch 2015). Endophytic bacteria not only escalate nitrogen fixation/phosphate solubilization but under stress conditions (abiotic and biotic), they mount the production of phytohormones and regulate the biosynthetic pathway of ethylene. Endophytes in plant system synthesize many biologically active novel compounds without any observable damage to the host tissue like alkaloids, terpenoids, steroids, peptides, poly-ketones, quinols, flavonoids, phenols, and insecticide azadirachtin (Kusari et al. 2012; Molina et al. 2012; Zinniel et al. 2002) antifungal compounds include cryptocandin, pestaloside, cryptocin, ecomycins, pestalopyrone, and pseudomycins. Endophytic microorganism increases plant resistance against the pathogen by inducing defense mechanisms, the so-called induced systematic resistance (ISR) (Zamioudis and Pieterse 2012). Another most significant and important mechanism for endophyte inhabitation in plants is the production of the extracellular enzyme exhibiting enormous industrial significance in different fields such as fermentation process and biotechnological applications. Some of the extracellular hydrolase enzymes augmented the plant responses to pathogenic infection (Leo et al. 2016). Endophytic strains of endophytic microflora are harnessed for commercialscale production as biofertilizers and biopreparations. Biofertilizers are defined as substances that contain living organisms tending to inhabit with the rhizosphere or the plant interior which are coalesced to seeds, plant surfaces, or soil. They increase the availability and supply of the nutrient which boost plant growth. The common bacteria’s, such as Azospirillum, Herbaspirrilum, Acetobacter, Azotobacter, and Azoarocus, have been successfully used as biofertilizers. Nowadays, there is a quest for microbial strains which can contribute to the development of bioinoculants, biofertilizers, and biopreparations, consequentially enhances the growth and yield of crop plants. Biopreparations are the products that originate from either living organisms or their metabolites, used in organic farming for environmental stress regulation. In the plant–soil interaction, there is a narrow region called as rhizosphere, which directly influenced by root microbiome and root secretion. This symbiotic association influenced the ability of the plant to absorb nutrients specifically phosphorus, nitrogen, iron, and potassium. In the soil symbiotic zone bacteria’s grow, which directly and indirectly enhanced the growth of plants and hence considered as plant growth-promoting rhizobacteria (PGPB)/bioinoculants/microbial inoculants. In the agricultural field, PGPB is considered a green alternative to boost

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sustainable soil fertility as well as plant growth (Tilak et al. 2005). PGPB supports the growth of plants through phosphorus solubilization, nitrogen fixation, absorption and assimilation of minerals/nutrients. These Endophytic bacteria also produce siderophore and many phytohormones which support the plant life in adverse stressful condition (Glick 1995; Bhardwaj et al. 2014; Pahari et al. 2016) (Table 14.1). Siderophores have potential roles and applications in various areas of environmental research due to their affinity in metal binding especially with iron. Chemically siderophores are the iron-containing low molecular weight chelating agents, showing specific affinity with ferric ions, therefore, siderophores can be termed as “Fe-biosensors.” They facilitate bioremediation, weathering of soil-mineral particles, and enhanced plant growth. Most of the aerobic and facultative anaerobic microorganisms like Pseudomonas, Azotobacter, Bacillus, Enterobacter, Serratia, Azospirillum, and Rhizobium (Glick et al. 1999; Loper and Henkels 1999; Pahari and Mishra 2017) synthesize siderophore under iron-limited conditions (Neilands 1981). As per research report, all microbes do not require iron and siderophores. There are some lactic acid-producing bacteria which showed poor growth in iron-containing medium because they don’t have iron regulating ribotide reductase enzyme. Iron is the fourth most abundant element on the earth, an essential micronutrient for plant growth, though deemed as most lacking micronutrients due to its insoluble nature of Fe+3 . The preliminary role of siderophores is scavenging of Fe. They also form complex molecules with other essential micro-elements like Mo, Mn, Co, and Ni in the environment and make them available for microbial cells (Bellenger et al. 2008; Braud et al. 2009a, b). There are no specific and defined procedures for the isolation of siderophores, as they differ substantially in their structures. Detection of siderophores can be finished by paper electrophoresis method whereas; structural characterization is best carried out by NMR and mass spectroscopy. In this chapter we will focus on the structure, functions, and applications of siderophores specifically in nutrient absorption by crop plants in the agriculture field.

14.2 Types of Siderophore At present nearly 500 siderophores are reported from selected microorganisms. A great variation is seen in siderophore structure from one species to another. Broadly such siderophore is classified into two (a) Microbial siderophore, and (b) Phytosiderophore. (a) Microbial siderophores: According to the oxygen ligands for Fe3+ organization bacterial siderophores can be differentiated into three main categories, namely, catecholate (i.e., enterobactin), carboxylates (i.e., rhizobactin), and hydroxamates (i.e., ferrioxamine B) (Matzanke1991). However, there is also a certain type of microbial siderophores that contain a mix of the main functional groups (i.e., pyoverdine) (Cornelis 2010). One such most common fungal siderophores is hydroxamates belonging to the ferrichrome family (i.e., ferrichrome), which is further divided into

Unknown Unknown Unknown Desferrioxamine

Escherichia coli

Pseudomonas putida

Micrococcus luteus

Streptomyces coelicolor

Ferrichromes) Ferricrocin Coprogens Fusigen

Ustilago sphaerogena

Aspergillus fumigates

Trichoderma sp

Fusarium sp

(B) Fungi

Ferribactin

Pseudomonas fluorescens

Name of siderophore ferrioxamines

(A) Bacteria

Hydroxamate type characteristics: • hydroxamate belongs to C(= O)N-(OH)R • -R: is an amino acid • hydroxamate siderophore forms a complex of hexadentate octahedral structure with Fe3+ form

Erwinia, Nocardia, Streptomyces, Arthrobacter, Chromobacterium and Pseudomonas

Siderophore-producing microbial cell

Type of siderophore

Table 14.1 List of different types of siderophore produced by different groups of microbes

(continued)

Diekmann and Zahner (1967)

Diekmann and Zahner (1967)

Wallner et al. (2009)

Emery (1971)

Saharan and Nehra (2011)

Cabaj and Kosakowska (2009)

Sayyed et al. (2005)

Kannahi and Senbagam (2014)

Maurer and Keller-Schierlein (1968)

Winkelmann (2007)

References

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Siderophore-producing microbial cell

Carboxylate type characteristics: Such siderophores exhibits hydroxy and carboxylate donor groups

Staphyloferrin B

Staphylococcus aureus

Paracoccus denitrificans

Staphyloferrin A

Parabactin

Agrobacterium tumefaciens

Staphylococcus hyicus Staphylococcus aureus

Agrobactin

Vibrio cholera

Rhizobactin

Vibriobactin

Bacillus cereus, Bacillus anthracis and Bacillus thuringiensis

Rhizobium meloti

Petrobactin Bacillibactin

Bacillus cereus, Bacillus anthracis

Bacillibactin

Bacillus anthracis Bacillus subtilis

Beasley et al. (2011)

Meiwes et al. (1990) Beasley et al. (2011)

Drechsel et al. (1995)

Dave et al. (2006)

Dave et al. (2006)

Saharan and Nehra (2011)

Wilson et al. (2006)

May et al. (2001)

Saharan and Nehra (2011)

Saharan and Nehra (2011)

Sayyed et al. (2005)

Salmochelins

Pyoverdine

References Saharan and Nehra (2011)

Name of siderophore Enterobactin (or enterochelin or cyclic trimester of 2.3-dihydroxy ben-zoylserine) First tricatechol siderophore

Salmonella enteric

Catecholate type E. coli, Aerobacter aerogenes, and Salmonella typhimurium (the most intensively analyzed siderophores) Characteristics: • Structure backbone of Catecholate siderophore is polyamine (a) peptide or (b) a macrocyclic lactone Pseudomonas aeruginosa

Type of siderophore

Table 14.1 (continued)

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five groups, depending on their side chain group hydroxamate (Renshaw et al. 2002; Winkelmann 2007). (b) Phytosiderophore: Iron is one metal, available in abundance in the soil, an essential microelement for plant growth but even then, the plant faces the deficit condition for this microelement. To escape such adverse conditions plant has secreted specific chelating compounds “Phytosiderophore.” Phytosiderophores (PS) are the organic substances (such as nicotinamine, mugineic acids (MAs), and avenic acid, etc.) secreted by the roots of plants of graminae family (e.g., wheat, rice, maize, sorghum, oat, barley, etc.) under Fe-deficient conditions (Mori and Nishizawa 1987). The Phytosiderophore can form organic complexes or chelates with Fe3+ and increase the movement of iron in soil (Ueno et al. 2007). The iron (Fe)-phytosiderophore complex enters the roots through an iron transporter channel present in the root plasma membrane and endorsed the efficiency of Fe mainly in the area having low soil Fe availability. The phytosiderophores are hexadentate ligands that coordinate Fe+3 with their amino and carboxyl groups (Singh et al. 2011). According to Wallace (1991) phytosiderophore are non-proteineous, low molecular weight acids released by the plants under the iron and zinc deficiency stress. The phytosiderophore mobilizes nutrient elements (like Fe, Zn, Mn, and Cu) from the soils to plant in deficient condition (Takagi et al. 1984). Fe-chelates are highly soluble and stable over a wide pH range. In comparison with the molecular mass of microbial siderophores (ranged 200–2000 Da) phytosiderophores are ranged between 500 and 1000 Da (Neilands 1981). Mugineic acid (MA) is the most common siderophore and the firstly identified in plants (Takemoto et al. 1978). The stability constant of the MAFe+3 complexes is very low as compared with the stability constant of ferrichrome, ferrioxamine B, and enterobactin microbial siderophores (Raymond et al. 1984; Schwarzenbach and Schwarzenbach 1963; Harris et al. 1979). Some important phytosiderophore which has been isolated from the gramineous plants are distichonic acid from Hordeum vulgare (beer barley) (Nomoto et al. 1981) avenic acid A from Avena sativa (oat). A plant releases phytosiderophore at higher amounts about a few hours (± 3 h) to the onset of the light period. Under continuous darkness or continuous light, the rate of release of phytosiderophore is lower. Further release of siderophores varies along the root and is most pronounced in the apical root zone compared to the other zones of the root. Morphologically highest uptake rates were found in highly branched root system; whereas the lowest uptake rates were found in the thicken root system (Romheld and Marschner 1990). Nature released of phytosiderophores is studied with the help of high-performance liquid chromatography (HPLC) (Mori et al. 1991). According to Cakmak et al. (1994) amount and composition of phytosiderophores are affected by plant age, type and properties of soil, root morphology, crop varieties, nutritional status of the plant, temperature, light duration, daytime vs light intensity. Releasing rate of phytosiderophores by plants differs between plant to plant species and is positively correlated with the plant resistance capacity to Fe deficiency.

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14.3 Shuttling Mechanism Through Siderophore Mediated Iron Transporter System Fe is considered as the key regulatory element of cellular metabolic pathway. It regulates the activity of many antioxidative enzymes like catalase, peroxidase (POD), ascorbate, and superoxide dismutase. Deficiency of Fe in plant system may affect oxidative defensive system and cause oxidative injury. Therefore, all the living beings are required a well-organized and controlled system of Fe absorption and utilization. Siderophore by forming a multi-complex system with the nutrient molecules play an important role in the transportation of ferric ions into the plant cell. Specific siderophore receptors are present on the cell membrane which helps in transporting the siderophore–iron complex to the cell interior.

14.4 Cell Membrane Siderophore Receptors There are different types of siderophore specific receptors present in different types of gram-positive and gram-negative bacteria. Gram-negative bacteria (e.g., Escherichia sp.) possess receptor specifically on the outer membrane that recognize the Fe (III)– siderophore complexes at the cell surface (Krewulak and Vogel 2008) whereas grampositive bacteria (e.g., Bacillus sp.), lacks the outer membrane and their receptor molecules. Therefore, periplasmic siderophore receptor helps in binding Fe (III)– siderophore complexes (Fukushima et al. 2013). Fec A and Fep A protein receptors are present on the outer membrane, whereas Ton B-Exb B complex siderophore receptor is present on the inner membrane. Fec CDE- Fep CDE- ATP dependent carrier molecules are present as an inner membrane and periplasmic transporting proteins.

14.5 Channel of Fe Transportation in Microbes and Plants When the siderophore is released from the cell, the membrane receptors protein binds with iron and forms iron–siderophore complex and transported into the cell via Fec A and Fep A (an outer membrane receptor), then it is transported to Fec CDE- Fep CDE an ATP-dependent transporter systems (or ABC-Transporter systems). Finally, siderophore–iron complex is released into the cytosol with the help of membrane receptor protein Ton B. In the cytoplasm, iron is released from the complex via hydrolytic breakdown in the presence of NADPH linked siderophore reductase and Ent ABCD protein. Such produced Fe++ does not have a high affinity with siderophore and it separates from the siderophore–iron complex. The released siderophores either get degraded or recycled by excretion through efflux pumping system (Table 14.2).

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Table 14.2 List protein Channel of Fe transportation in microbes Model system

Location

Receptor proteins

References

Bacteria

An outer membrane receptor

Fec A and Fep A

Sajeed Ali and Vidhale (2013)

An inner membrane receptor

Fec CDE- Fep CDE (an ATP dependent transporter systems/or ABC-Transporter systems) and Ton B

Sajeed Ali and Vidhale (2013)

Cytosol

Ent ABCD protein

Sajeed Ali and Vidhale (2013)

Fungi

Siderophore mediated Fe transport system Mechanisms

Process

References

The shuttle mechanism • Fe-siderophore complex is Ardon et al. (1998) transported across the cell membrane and released the Fe+3 ions from the ligands and reduced by the reductive enzymes • Recycle the free siderophore • e.g., transporting ferrichrome in Ustilago maydis The taxicab mechanism

• Fe+3 extracellular siderophore is transferred across the cell membrane to intracellular membrane ligands e.g., Rhodotorula species

The hydrolytic mechanism

• After the transportation of Adjimani and Fe+3 siderophore complex Emery (1988) inside the cell, it undergoes reductive and degenerative steps and release the Fe+3 • Fe+3 is then reduced into Fe+2 and the siderophore is further released out e.g., uptake of Fe+3 tri-acetyl-fusarinine complexes by Mycelia sterilia

Winkelmann and Huschka (1987)

(continued)

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Table 14.2 (continued) Model system

Location

Receptor proteins

The reductive mechanism

• Fe+3 –siderophore complex Ecker and Emery is not transported across (1983) the cell membrane • Reduction of Fe+3 into Fe+2 occurs at the surface of the cell membrane • Reduced Fe is taken up by the cell e.g., uptake of Fe+3 from ferrichrome by Ustilago sphaerogena

References

14.6 Approaches Use in Fe and Zn Acquisition by Plants Plants grown in alkaline or calcareous soil generally showed chlorosis types of nutritional disorder due to low soil solubility for Fe and Zn ions. Fe absorbing and storing mechanisms in higher plants have been categorized into two types as Type I and II. 6.1 Type I plants (dicotyledons and non-graminaceous monocotyledons): These plants respond to Fe paucity by extruding the protons from the plasma membrane of the root surface. Fe+3 form reduced into the soluble Fe+2 form on the root plasma membrane and then penetrates inside the root cell through the specific Fe+2 transporter molecules (Tagliavini and Rombola 2001). 6.2 Type II plants (graminaceous species): These plants synthesize and secrete Fe-chelating substances like mugineic acids (MAs) from their roots, which increases the dissolving efficiency of Fe compounds in the rhizospheric zone (Marschner et al. 1986). After this, iron molecules are transported across the plasma membrane in the form of complex molecule (PS-Fe+3 ) through a specific transport system without the reduction reaction. The quantity of mugineic acid synthesized and secreted into the rhizosphere may fluctuate among species to species (Xiong et al. 2013). The amount of MAs secreted correlates positively with the ability of the plants to tolerate Fe deficiency (Xiong et al. 2013).

14.7 Occupations of Siderophore-PGPR in Crop Field 7.1 Siderophore as a Plant Growth Promoter: Siderophores are used in agricultural field as an ecofriendly and alternative approach to reduce the adverse effect of hazardous chemical pesticide. Recently many species of Pseudomonas have been identified that can enhances plant growth by producing pyoverdine, hydroxamate type of siderophores (Kloepper et al. 1980; Gamalero and Glick 2011; Mahmoud and Abd-Alla2001). Bacteria like Azadirachta indica produce ferrioxamines siderophore

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in rhizosphere region, increases Fe transportation efficiency within the plant for the root and shoot growth (Verma et al. 2011; Crowley 2006). Gangwar and Kaur (2009) and Rungin et al. (2012) isolated some bacteria [Escherichia coli from ryegrass (Loliumperenne sp.)] and an endophytic fungus Streptomyces sp. from the roots of Thai jasmine rice that enhances plant growth and significantly improved the root and shoot biomass and lengths. It has been correlated that excessive accumulation of heavy metals is toxic for most of the plants and responsible for the contamination of soil which decreases soil fertility and soil microbial activity (McGrath et al. 1995). In this context, hydroxamate type of siderophore present in soil will play an important role to immobilize the metals and act as plant growth promoter. 7.2 Siderophore as inhibitor for phytopathogenic attack: Siderophore acts as an inhibitor for phytopathogenic attacks and restrains the growth of phytopathogens. Molecules of siderophores bind with iron and make it unavailable for the plant pathogens (Beneduzi et al. 2012; Ahmed and Holmstrom 2014). Siderophores synthesized by Pseudomonas and Bacillus sp. (a type of rhizobacteria) inhibited the attack of Phytophthora parasitica (Seuk et al.1988), Fusarium oxysporum veridianthi (Buysens et al. 1996), Pythium ultimum (Hamdan et al. 1991), and Sclerotinia sclerotiorum (Mc Loughlin et al. 1992). For example: different strains of Pseudomonas fluorescens (like A1, BK1, TL3B1) act as a biological controlling agent against Erwinia carotovora and Fusarium oxysporum. F. oxysporum causes wilt diseases in potatoes (Kloepper et al. 1980; Schippers et al. 1987). 7.3 Siderophore as Bioremediation: There is release of heavy metals and metalloids from petroleum industry, chemical industry, etc., which contaminates the soil and water and for this siderophores is of prime prominence for metal bioremediation apart from binding with ferric iron, siderophores also regulate the gelatinization the other toxic metals, e.g., Cr3+ , Al3+ , Cu2+ , Eu3+ , and Pb2+ via the production of pyoverdine siderophore (P. aeruginosa), azotochelin (Azotobacter vinelandii), schizokinen, and N-di-oxyschizokinen production (Bacillus megaterium) stimulates molybdenum and aluminium biosynthesis, respectively (Braud et al. 2009a, b; Duhme et al. 1998; Hu and Boyer 1996). Specific siderophores showed very strong ligands affinity with specific metallic ions and form siderophore–metal complex molecule, which depends upon the ligand functionalities and siderophore–metal complex formation (Hernlem et al. 1999). 7.4 Endophytes and their role in Fe (iron) management in soil: It has been iterated that iron (Fe) is an essential element for plant growth and development. PGPR can increase Fe absorption by plants through reduction of Fe (III) to Fe (II) at the root surface. The bacterial strains with high Fe (III) reduction ability were able to stimulate plant growth in vitro and on a broad level. Plants grown in inoculated soil were generally bigger and with higher Fe content than those grown in sterilized soil. This contributes significantly due to Fe absorption by plants likely through increased Fe (III) reduction in the rhizosphere Valencia-Cantero et al. 2007. The role of bacterial endophytes in the acquisition of iron (Fe) solubilization and acquisition systems by plant-associated microbes with respect to improving plant growth and health used to enhance the supply of iron often limiting nutrients to the host plant (Chhabra and Dowling 2017). Siderophore-producing endophytes Arthrobacter sulfonivorans

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DS-68 and Enterococcus hirae DS-163 enhanced biofortification of grains with Fe and yield in four genotypes of wheat (Triticum aestivum L.) in soils with low and high available Fe content. Endophyte inoculation increases the surface area, volume, length of roots, and the number of root tips. Such siderophore-producing endophytes can be recommended as bioinoculants to mitigate iron deficiencies in the soil and enhance crop productivity (Singh et al. 2020).

14.8 Conclusion Siderophore-producing plant growth-promoting rhizobacteria (PGPR) are microbes that colonize in the rhizospheric zone of the crop plant and significant increases the agricultural yield in the stressed soil. Phytosiderophores production acts as a lifesaving mechanism in the plants by substantiating the function of Fe and Zn, in Fe and Zn deficiency soil. Pytosiderophores increases 5–10 times mobilization of Fe and Zn under stress conditions. They chelated Fe3+ irons and reduce into the Fe2+ form. Using the biotechnological approaches, tools, and techniques, we can develop transgenic field crops, which possess phytosiderophores secretion responsible gene, resulting in the increase of the minerals absorption in nutrient-deficient conditions and thus increasing the crop yield. In the current scenario, this kind of organic farming practices with microbial diversity has added significant consideration to enhance the crop yield. Applications of the organic manures increase soil microbiome, which directly or indirectly increases soil fertility in the agricultural field, beside this, they also inhibit iron-dependent soil-borne phytopathogens. Hence siderophores will play an importation role when applied in the agriculture field, increasing the plant growth and biomass, enhancing the productivity and crop yield.

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Chapter 15

Conclusion Dinesh Kumar Maheshwari

The scientists so far have paid much attention to the understanding of plant beneficial free-living and symbiotic bacteria and only recently realized to look deeper into those microorganisms inhabiting inside the plant tissues and remain asymptomatic (Nerva et al. 2019). The symptomless plants bear certain group of microorganisms which play a vital role in growth and health, promotion of the plants, named as “Endophytes.” These microorganisms include bacteria, actinobacteria, and fungi having the main source of agrobiological interest. They create a host plant–endophyte relationship to provide a beneficial alternative for synthetic fertilizers and pesticides due to their diverse potential for sustainable agroecosystem. Information is given about endophytic microorganisms particularly bacteria for acting as a source of N, P, K, Zn, Fe, S, etc., for enriching the soil in a balanced ecosystem (Pandey et al. 2018). Thus, the major emphasis has been laid down on the promising role of endophytes for green agriculture and to understand them for evolving in plant–microbe interaction processes in the holobionts. The endophytic microbial communities are intimately associated with a different degree with cells and tissues of the plant and form a microbial hub composed of strongly interconnected taxa that grow under the neutral benefit. We undoubtedly made great advances in the commercialization of biofertilizers as biopesticides in bioremediation and microbial inoculants. The advancement of knowledge realized us that endophytes living in plant tissues are significantly more potential to mineralize soil nutrients than free-living bacteria . It has given us a wake-up call to reboot our scientific quest and pay much more attention to those hidden microbes and turn toward mother nature for solutions to the problems of today, i.e., lack of food for humans and animal feed (Arora 2018). The past two D. K. Maheshwari (B) Department of Botany and Microbiology, Gurukula Kangri Vishwavidyalaya, Haridwar, Uttarakhand, India e-mail: [email protected] © Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4_15

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decades were evidenced by a growing interest in the investigations aimed at origins, interactions of endophytes, as a new source of asymptomatic establishment in the plants opening horizon of studies in agrobiology. These microorganisms are not limited to bacteria and actinobacteria, even some important groups like fungi are also involved in the production of bioactive compounds. Their beneficial association of mycorrhizal fungi to boost plant growth and productivity enhancement was involved in the book venture. For all these purposes, minimal nutrient uptake and balanced accumulation modulate is an utmost requirement which only met-out by the exploitation of different endophytes genera in crop production (Jayakumar et al. 2019; Guo et al. 2019). Similar to biofertilizers, the commercialization of endophytic organisms as bioinoculants is a reality of the hour and covered in many chapters of the book, this, however, explores the use of the more efficient organisms concerning their potential in crop productivity enhancement via a suitable and sustainable way. This involves resistance mechanisms to the major abiotic and biotic stresses which often create confidence among the farmers (Firrincieli et al. 2020). But to isolate such multifarious endophytes, we have to go back into the biblical era to the present era. For example, dung as a novel source of microbes, if amended with its inhabited bacteria, acted as a catalyst for augmenting the crop productivity and soil fertility for sustainable nutrient management practices. Sometimes nutrient deprivation specifically iron may be proved most beneficiary in the mechanism of plant disease control. This also includes a couple of chapters in the last of the book. On the other hand, endophytes also provide a firm substitute for lack of phosphorus, zinc, potassium, nitrogen, etc., and besides their application, support soil biology (Arya et al. 2020). Considering such viable strategies, the endophytic microorganisms are now established as good as pure chemical fertilizer for boosting crop yield. Harnessing beneficial endophytic microorganisms for delivering macro and micronutrients may provide new trends and prospects to agroeconomy if it meets out the requirements to apply as a formulation product for a wider application similar to the free-living plant growth-promoting rhizobacteria (Etesami and Maheshwari 2018). This complex association is evident in the information provided in this volume. Almost all plants inhabit some endophytic microorganisms and only a few have been studied so far—the diverse plants of different habitats such as temperate, tropical zones. In the last, this is to say that characterization of endophytes using advanced tools can help in finding more bacterial inoculants. Modern tools and techniques of including metagenomics, proteosomes, metabolome, transcriptomes, etc., may help in defining characteristics of endophytes for better improvement of crop productivity. Scientists may reap benefits of day to day increasing publications on endophytes.

15 Conclusion

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References Arora NK (2018) Environmental sustainability—necessary for survival. https://doi.org/10.1007/s42 398-018-0013-3 Arya R, Pandey C, Dheeman S, Aeron A, Dubey RC, Maheshwari DK, Lei C, Ahmad P, Bajpai VK (2020) Fertilizer adaptive bacteria Acidovorax valerianellae and Sinorhizobium fredii in integrated nutrient management of pigeon pea (Cajanus cajan L.). Afr J Bot. https://doi.org/10. 1016/j.sajb.2020.03.018 Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Safe 156:225–246 Firrincieli A, Khorasani M, Frank AC, Doty SL (2020) Influences of climate on phyllosphere endophytic bacterial communities phyllosphere endophytic bacterial communities of Wild poplar. Front Plant Sci 11:203 Guo Y, Gao P, Li F, Duan T (2019) Effects of AM fungi and grass endophytes on perennial ryegrass Bipolaris sorokiniana leaf spot disease under limited soil nutrients. Euro J Plant Pathol 154(3):659–671 Jayakumar A, Krishna A, Mohan M, Nair IC, Radhakrishnan EK (2019) Plant growth enhancement, disease resistance and elemental modulatory effects of plant probiotic endophytic Bacillus sp. Fcl1. Probiot Antimicrob Prot 11(2):526–534 Nerva L, Turina M, Zanzotto A, Gardiman M, Gaiotti F, Gambino G, Chitarra W (2019) Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants. Environmen Microbiol 21(8):2886–2904 Pandey C, Negi YK, Maheshwari DK, Rawat D, Prabha D (2018) Potential of native cold tolerant plant growth promoting bacilli to enhance nutrient use efficiency and yield of Amaranthus hypochondriacus. Plant Soil 428(1–2):307–320

Index

A Abscisic acid, 189 ACC, 49–51, 54, 56, 58, 188, 190. See also 1-aminocyclopropane, 1-carboxylic acid ACC deaminase, 49–51, 54, 56, 58. See also ACC Acinetobacter, 41, 45, 47, 55 Actinobacteria, 6, 229, 231, 232, 234–237, 239 Actinobacterial endophyte. See Actinobacteria Actinomycetales, 133 Adenosine triphosphate, 210 Agricultural production, 4 Agrobacterium, 158 Agrobiology, 332 Agrochemicals, 207, 209, 210, 293, 294, 296, 298, 301 Agroeconomy, 332 Agroecosystem, 331 Alkaloids, 141 AMF. See Arbuscular mycorrhizal fungi 1-aminocyclopropane, 1-carboxylic acid, 4 Amycolatopsis, 231, 233 Anaerobic fermentation, 81, 93 Animal feed, 331 Animal waste, 81 Ansamitocin, 135 Antagonist, 127 Antibiotic production, 139, 230 Antibiotic(s), 14, 36, 51, 207–209 Anticancer, 124 Antifungal, 124 Antimicrobial, 124 Antioxidant, 124

Apatite, 37 Apoptosis, 124 Arabidopsis, 135 Arbuscular mycorrhiza, 6 Arbuscular mycorrhizal fungi, 230 Arthrobacter, 135, 231–233, 235–237 Ascorbic acid oxidase, 18 Auxin, 124, 189, 207, 210, 298 Azadirachta indica, 323 Azospirillum, 316, 317 Azotobacter, 4, 298, 302, 304

B Bacillomycin, 165 Bacillus, 4, 15, 16, 18, 41, 44–47, 50–52, 54– 57, 79, 80, 82–84, 93, 158–160, 163– 173, 211, 213, 214, 216, 218, 271, 274–277, 298–300, 302–304, 306 amyloliquefaciens, 165–168, 170, 172 cereus, 165 megaterium, 165, 170–172 pumilus, 165, 167, 168, 172 Bacterial blight, 236 Bacteriocins, 159, 167 Basidiomycota, 42, 48 BCA. See Biological control agents Betaproteobacteria, 214 Bifidobacterium, 80 Bioactive metabolic compounds, 193 Bioavailability, 138 Biocontrol, 4, 19, 230 Biodiesel, 215 Biodiversity, 133, 158 diversity, 162, 163, 170 Biofertilizers, 210, 331

© Springer Nature Switzerland AG 2021 D. K. Maheshwari and S. Dheeman (eds.), Endophytes: Mineral Nutrient Management, Volume 3, Sustainable Development and Biodiversity 26, https://doi.org/10.1007/978-3-030-65447-4

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336 Biofilms, 159, 162 Biofuel, 216 Bio-gas, 79, 81, 92, 93 biogas production, 81, 82. See also gobar gas Bioinformatics, 8 Biological control. See Biocontrol Biological control agents, 11–13, 22, 127 Bioremediation, 8, 181, 182, 192, 324 Biotechnology, 8, 207, 209 Brassica napus, 43 Brazilian mangroves, 218 Buffalo dung, 78, 81, 89 Burkholderia, 14, 18, 41, 44, 45, 49, 51, 54, 58, 59, 158, 298, 300, 302–304 Burkholderiales, 133

C Camptothecin, 135, 141 Castor, 215 Catecholate siderophores, 236 Cellulomonas, 231, 232, 236, 237 Cell wall, 236 Cepabactin, 139 Cereals, 158 Charcoal, 79 Chemotaxis, 132 Chickpea, 278 Chitinases, 159, 207, 208 Chloramine –T, 234 Chlorophytum, 41 Chryseobacterium, 272, 276–278 Citrobacter, 79, 80 Clavicipitaceae, 127 Claviciptaceous endophytes, 42 Climate change, 247, 248, 259 Coffea arabica, 212–214 Colletotrichum, 126, 127, 130, 141, 144 Compost, 297, 304 Comptotcin, 124 Convolvulaceae, 135 Corynebacterium, 231, 232 Cow dung, 90 dung, 79, 81, 83, 84, 86–89, 92, 93 Cow urine, 82 Cronobacter, 214 Crop-fertilization, 268 Crop production, 293, 297, 301 Crop productivity, 78, 86, 267, 332 Crop protection. See Biocontrol Curtobacterium, 42, 50, 231–233, 238, 239

Index Cytokinins, 124, 189, 298

D DAPG 2,4-diacetylphloroglucinol, 14 2,4-diacetylphloroglucinol, 14 Diazotrophic endophytes, 272 disease control. See Biocontrol Diterpene, 141

E Ecological niche, 36 Ecomycin, 134 Ecosystem, 78, 87, 94, 207, 210, 217, 331 Endophytes, 3, 12–14, 16–24, 36, 38–43, 45–53, 57, 59, 60, 159, 160, 164, 181, 183, 207, 208, 210, 211, 247–249, 251, 253, 254, 257, 259, 331, 332 colonization, 160–162, 166, 167, 173 Eucalyptus–endophytic bacteria, 164 facultative endophytes, 160, 184 migration, 162 obligate endophytes, 184 oligate endophytes, 181–185, 191–195 penetration, 162 Endophytic fungi, 6, 247 Endophytic rhizobacteria, 267 Endosphere, 36, 38, 47, 50, 58, 273, 279 Enterobacter, 79, 80, 82, 83, 158, 214, 218, 271, 274, 277, 278 Enterobacteriales, 133 Enterobactin, 317, 320 Environmental pollution, 268 Epichloë, 249, 250, 253–256, 258 Epoxy-janthitrem, 141 Ergopeptine, 141 Ergosterol, 139 Ergovaline, 141 Erwinia, 212, 214 Escherichia, 79, 83 Ethylene, 17, 23 Euryarchaeota, 80 Exopolysaccharide, 159 Extracellular enzymes, 190 amylases, 190 cellulases, 190 Chitinase, 190 dehydrogenase, 190 lipases, 190

Index F Falvobacterium, 278 Fengycin, 165 Fermentation, 140 Ferrichrome, 317, 320, 322, 323 Ferrioxamines, 8 Fertilizers, 5, 78–80, 82, 88, 90–93, 158, 163, 207, 209, 210, 219, 220, 247, 249, 254, 267, 269, 272, 274, 281, 293, 294, 297, 301, 302, 306 inorganic fertilizers, 78, 91, 92 NPK, 90–92 Ferula songorica, 132 Firewood, 79 Firmicutes, 12, 158, 214 Flavobacteriales, 133 Flavonoids, 132 Fluorescence in situ hybridization, 40 Food security, 294, 296, 307, 315 Free-living bacteria, 331 Fuelwood, 78, 79 Funneliformis mosseae, 231, 233, 235, 238, 240 FYM, 297 G GA3 Gibberellin, 239 Gammaproteobacteria, 214 Genomic, 181, 182, 193, 195 Gibberellic acid, 46, 50 Gibberellin, 124, 189, 239, 298 Global warming, 268 Glomus mosseae, 231, 232, 234, 235, 237– 239 Gluconacetobacter, 270, 271, 276 Gluconic acid, 236 Glycyrrhizic acid, 138 Gobar gas, 81 Gram-positive, 229, 230 H HCN, 298 Herbaspirrilum, 316 Homeostasis, 132, 256 Hydrogen cyanic (HCN) acid production, 4 Hydrogen cyanide, 190 Hydrolytic enzymes, 247, 254 amylases, 84 cellulases, 84 gelatinase, 84 urease, 84

337 xylanases, 84 Hydroxamate siderophores, 236 Hydroxyapatite, 37 Hydroxymate, 8 I IAA. See Auxin IAA production. See Auxin Illumina pyrosequencing, 41 Immobilization, 209, 211 Indole-3-acetic acid, 42, 50, 65 Induced systemic resistance, 4, 191, 297. See also ISR Industrial agriculture, 207 Inorganic phosphorus, 37 Intrasporangium, 231, 232, 237 Isoflavonoids, 132 ISR, 14, 17, 22–26. See also Induced systemic resistance J JA-signalling pathways, 17 Jasmonic acid, 17, 189, 197 Jatropha, 215, 216 Jatropha curcas, 215 K Kakadumycins, 134 Klebsiella, 79, 83, 158, 214, 216 Kluyvera, 79 Kosakonia, 214 KSB, 272, 273. See also Potassium solubilizing bacteria Kurthia, 214 L Lactobacillus, 79 Land degradation, 268 Lateral roots, 132 Leifsonia, 231, 232, 235–239 Lenticels, 132 Livestock, 78, 79, 93 Livestock dung, 78 Lysinibacillus, 214 Lytic enzyme, 36 M Macronutrients, 294, 300, 304 Mahonia fortune, 139

338 Maize cereals, 158, 159, 163–165, 170, 171, 173 MALDI-TOF, 214 Malonic acid, 236 Mangrove forests, 217 Maytansinoid, 135 Medicago truncatula, 135 Medicine, 8 Metabolomics, 181, 182, 193, 195 Metagenomics, 40, 41 Metatranscriptomic, 182 Methanobacterium, 80, 82 Methanobrevibacter, 80 Methanomicrobium, 80 Methanosarcina, 80, 82 Microbacterium, 41, 42, 54, 55, 214, 216, 271, 274, 276, 278, 300 Microbial inoculants, 207 Micrococcus, 275, 278 Micronutrients, 236, 247, 251, 294, 299, 304 Millet, 158, 160, 164 Mineralization, 207, 209, 217 Mineral nutrients acquisition, 267, 269, 278– 280 Mineral nutrient uptake, 247 Mineral phosphate, 37 Minerals, 36, 37, 78, 79, 85, 208, 249, 251, 253, 272, 306, 317, 325 Mineral solubilization, 254 Modern agriculture, 11 Morgarella, 79 Municipal wastes, 138 Mycobacterium, 231, 233, 238, 239 Mycoparasitism, 130 Mycorrhiza, 231–235, 237, 238 Mycorrhizal fungi, 332

N Nif H, 42 Nitrogen fixation, 4, 42, 49, 50, 55 Nocardia, 231, 232, 237 Nocardioides, 231 NodD, 42 NUE. See Nutrient use efficiency Nutrient-deficiency, 267 Nutrient management, 78 Nutrient solubilization, 247 Nutrients replacement, 248 Nutrient uptake, 293, 298, 300, 302–304, 307 Nutrient use efficiency, 5, 301, 302

Index O Organic manures, 5 Oryza sativa, 240 Oxalic acid, 236 Oxidative stress, 39 Oxyapatite, 37 P Paenibacillus, 158, 213, 217 Pantoea, 16, 158, 213, 214 Parasitism, 19 Pasteurella, 79 Pathogenesis-related gene. See PR gene PCR, 186 Penicillium skrjabinii, 139 Peroxidase, 18, 321 Pesticides, 207, 209, 219, 222 Pest-management, 12 PGPB. See PGPR; Plant growth-promoting rhizobacteria PGPR, 85, 296, 297, 299, 300, 302, 303, 305. See also Plant growth-promoting rhizobacteria Pharmaceutical, 6 Pharmacology, 181, 182, 194 Phenazine, 139 Phenylalanine ammonia-lyase, 18 Phosphate buffer saline, 234 Phosphate solubilization, 4, 35, 36, 42, 45– 50, 54, 55, 58–60, 208, 210–212, 214, 216–219 Phosphate-solubilizing bacteria, 207, 211 Phosphate-solubilizing microbes, 37, 46, 304 Phosphatic fertilizers, 35–37 Phosphorus. See Phosphorus solubilization Phosphorus cycle, 208, 211 Phosphorus deficiency, 35, 36, 44 Phosphorus solubilization, 43, 47, 188, 209, 212, 217, 317 Phytoextraction, 138 Phytohormone production, 4 Phytohormones, 159, 298 Phytomining, 138 Phytopathogens, 182, 189, 191, 192, 207, 208 Phytophthora, 17, 22, 23 Phytoremediation, 132, 138, 181, 182, 192, 194 Phytosiderophore, 317, 320 Phytotoxicity, 132 Plant-fungal symbioses, 253 Plant growth hormones, 297

Index Plant growth-promoting bacteria, 158, 159, 297–299 Plant growth-promoting rhizobacteria, 8, 332. See also PGPR Plant growth promotion, 181, 187, 190 Plant immunity, 36 Plant-microbe interaction, 4 Plant microbiome, 267, 269, 280 Podophylotoxine, 124 Polymerase chain reaction, 186 Polyphenol oxidase, 18 Potassium solubilization, 273 Potassium solubilizing bacteria, 272 Potato diseases, 140 Powdery mildew, 140 Pramine, 141 PR gene, 18 Propagation, 139 Propionibacterium, 231 Propionic acid, 236 Proteases, 159 Proteobacteria, 158, 184 Proteomics, 181, 193 Providencia, 79 PSB, 273, 274. See also P solubilizing bacteria Pseudomonadales, 133 Pseudomonas, 4, 14–16, 24, 39, 41, 42, 44– 47, 51, 52, 54–57, 59, 79–84, 158, 211, 212, 214, 271, 272, 274–277, 298–300, 302–304, 306 Pseudomycins, 134, 316 Pseudonocardia, 231, 233, 235 Pseudoxanthomonas, 278 PSM, 37. See also Phosphate-solubilizing microbes P solubilization index, 218 P solubilizing bacteria, 273 Pyoverdine, 8 Pyrosequencing, 41, 133 Pyrrolizidine, 141 Pyrrolnitrin, 14, 139 Q Quorum sensing, 39, 58 R Reactive oxygen species, 18. See also ROS Reclamation, 216 Remediation. See Bioremediation Rhizobacteria, 267–280 Rhizobia, 4

339 Rhizobiales, 133 Rhizobium, 158, 214, 217 Rhizoctonia solani, 139 Rhizophagus intraradices, 236 Rhizophagy cycle, 213 Rhizosphere, 36, 38, 39, 41, 48, 49, 53, 56– 58, 60, 160–164, 170, 171, 253, 254, 256, 264 Rice cereals, 158, 160, 165, 170 Ricinus communis, 215 Rock phosphates, 36 Root-nodulating. See Rhizobia Root radical, 132 ROS, 18 Ryegrass, 135

S Salicylic acid, 17 SAR, 17. See also Systemic acquired resistance SA-signalling pathway, 17 Secretomes, 195 Sediments, 138 Siderophore production, 4, 50, 54, 55, 277, 278 Siderophores, 8, 36, 207–209, 214, 218, 247, 250, 253, 255, 256, 259, 277, 317, 323, 324 Soil ecology, 4, 207 Soil fertility, 5, 78, 84–87, 89–91, 293, 294, 296, 297, 304, 307 Soil microbiomes, 207 Soil microorganisms, 4 Soil phosphorus, 37 apatite, 37 hydroxyapatite, 37 oxypatite, 37 Soil-P solubilization, 254 Soil regeneration cycle, 247 Soil toxicity, 79 Sorghum, 158, 160 Sphingomonadales, 133 Sphingomonas, 42, 158 Spore-forming Bacillus. See Bacillus Staphylococcus, 158, 166, 214 Stenotrophomonas, 18, 41, 51, 52, 54–56, 272, 276, 277 Stomata, 132 Streptomyces, 230–233, 235–238, 240, 242 Streptosporangium, 231, 232, 237 Streptoverticillium, 231, 232, 237

340 Sugar beet, 133 Sustainable agriculture, 35, 267, 280 Sustainable farming model, 247 Sustainable soil management, 248 Swine manure, 89, 92 Symbiotic mutualism, 182 Systemic acquired resistance, 4. See also SAR

T Tannins, 130 Terpenoids, 132 Transcriptomic, 181, 193 Trichome, 132

V Vermicompost, 297 Verticillium dahlia, 14 Vitamins, 124 VOC, 16. See also Volatile organic compounds VOCs, 24. See also VOC Volatile organic compounds, 16

Index HCN, 159, 166, 167

W Waksman’s agar, 233, 234 Wheat cereals, 158, 159

X Xanthomonadales, 133 Xanthomonas campestris, 16 Xanthomonas campestris, 16 Xylanolytic bacteria, 84 Xylaria, 127

Z Zinc solubilization, 235, 236, 274, 277 Zn solubilizing bacteria, 274 Zn uptake, 274, 277 ZSB, 274, 277. See also Zn solubilizing bacteria Zygomycota, 42